From genetic diversity and structure to conservation: Genetic signature of recent population declines in three mouse lemur species (Microcebus spp.)

Biological Conservation

Volumn 141, Issue 5, 2008, Pages 1257-1271

  Olivieri, Gillian L ^a   Sousa, Vitor ^b,c   Chikhi, Lounès ^b,d   Radespiel, Ute ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

^d École Nationale de Formation Agronomique   (France)

Author keywords

Conservation; Demographic history; Habitat fragmentation; Madagascar; Microsatellites; Population structure

Indexed keywords

ANTHROPOGENIC EFFECT; CONSERVATION; ENDANGERED SPECIES; GENETIC DIFFERENTIATION; GENETIC STRUCTURE; GENETIC VARIATION; GEOGRAPHICAL VARIATION; HABITAT FRAGMENTATION; HUMAN SETTLEMENT; LANDSCAPE CHANGE; POPULATION DECLINE; PRIMATE; RARITY;

INDIAN OCEAN; INDIAN OCEAN ISLANDS; MADAGASCAR;

LEMUR; MICROCEBUS; MICROCEBUS RAVELOBENSIS; STREPSIRHINI;

EID: 44149100979     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2008.02.025     Document Type: Article

References (83)

1. Banks S.C., Lindenmayer D.B., Ward S.J., and Taylor A.C. The effects of habitat fragmentation via forestry plantation establishment on spatial genotypic structure in the small marsupial carnivore, Antechinus agilis. Molecular Ecology 14 (2005) 1667-1680
2. Beaumont M.A. Detecting population expansion and decline using microsatellites. Genetics 153 (1999) 2013-2029
3. Beaumont M.A. Conservation Genetics. In: Balding D.J., Bishop M., and Cannings C. (Eds). The Handbook of Statistical Genetics. second ed. (2003), John Wiley, New York 751-792
4. Bellemain E., Nawaz M.A., Valentini A., Swenson J.E., and Taberlet P. Genetic tracking of the brown bear in northern Pakistan and implications for conservation. Biological Conservation 134 (2007) 537-547
5. Burgess N.D., D'Amico Hales J., Ricketts T.H., and Dinerstein E. Factoring species, non-species values and threats into biodiversity prioritisation across the ecoregions of Africa and its islands. Biological Conservation 127 (2006) 383-401
6. Burney D.A. Late quaternary stratigraphic charcoal records from Madagascar. Quaternary Research 28 (1987) 274-280
7. Burney D.A. Pre-settlement vegetation changes at Lake Tritrivakely, Madagascar. Paleoecology of Africa 18 (1987) 357-381
8. Burney D.A. Rates, patterns, and processes of landscape transformation and extinction in Madagascar. In: MacPhee (Ed). Extinctions in near time: causes, contexts, and consequences (1999), Kluwer Academic/Plenum Publishers, New York 145-164
9. Burney D.A., Burney L.P., Godfrey L.R., Jungers W.L., Goodman S.M., Wright H.T., and Jull A.J.T. A chronology for late prehistoric Madagascar. Journal of Human Evolution 47 (2004) 25-63
10. Caizergues A., Rätti O., Helle P., Rotelli L., Ellison L., and Rasplus J.-Y. Population genetic structure of male black grouse (Tetrao tetrix L.) in fragmented vs. continuous landscapes. Molecular Ecology 12 (2003) 2297-2305
11. Campbell G. The state and precolonial demographic history: the case of nineteenth-century Madagascar. Omaly sy Anio 29-32 (1989) 189-222
12. Chikhi L., and Bruford M.W. Mammalian population genetics and genomics. In: Ruvinsky A., and Marshall Graves J. (Eds). Mammalian Genomics (2005), CABI Publishers, UK 539-583
13. Cornuet J.M., and Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144 (1996) 2001-2014
14. Craul M., Zimmermann E., Rasoloharijaona S., Randrianambinina B., and Radespiel U. Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species. BMC Evolutionary Biology 7 (2007) 83
15. Curtis J.M.R., and Taylor E.B. The genetic structure of coastal giant salamanders (Dicamptodon tenebrosus) in a managed forest. Biological Conservation 115 (2003) 45-54
16. Dewar R.E. Relationsship between human ecological pressure and the vertebrate extinctions. In: Goodman S.M., and Benstead J.P. (Eds). The Natural History of Madagascar (2003), The University of Chicago Press, Chicago 119-122
17. Dewar R.E., and Wright H.T. The culture history of Madagascar. Journal of World Prehistory 7 (1993) 417-466
18. Di Rienzo A., Peterson A.C., Garza J.C., Valdes A.M., Slatkin M., and Freimer N.B. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences USA 91 (1994) 3166-3170
19. Dunham A.E., Erhart E.M., Overdorff D.J., and Wright P.C. Evaluating effects of deforestation, hunting, and El Niño events on a threatened lemur. Biological Conservation 141 (2008) 287-297
20. Evanno G., Regnaut S., and Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14 (2005) 2611-2620
21. Ewens W.J. The sampling theory of selectively neutral alleles. Theoretical Population Biology 3 (1972) 87-112
22. Felsenstein J. Estimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. Genetical Research 59 (1992) 139-147
23. Ferraz G., Russel G.J., Stouffer P.C., Bierregaard Jr. R.O., Pimm S.L., and Lovejoy T.E. Rates of species loss from Amazonian forest fragments. Proceedings of the National Academy of Sciences USA 100 (2003) 14069-14073
24. Fredsted T., Pertoldi C., Olesen J.M., Eberle M., and Kappeler P.M. Microgeographic heterogeneity in spatial distribution and mtDNA variability of gray mouse lemurs (Microcebus murinus, Primates: Cheirogaleidae). Behavioural Ecology and Sociobiology 56 (2004) 393-403
25. Ganzhorn, J.U., Goodman, S.M., Dehgan, A., 2003. Effects of forest fragmentation on small mammals and lemurs. In: Goodman, S.M., Benstead, J.P. (Eds.), The Natural History of Madagascar, pp. 1228-1234.
26. Gasse F., and Van Campo E. A 40,000-yr pollen and diatom record from Lake Tritrivakely, Madagascar, in the southern tropics. Quaternary Research 49 (1998) 299-311
27. Gelman A., and Rubin D.B. Inference from iterative simulation using multiple sequences. Statistical Science 7 (1992) 457-511
28. Gelman A., Carlin J.B., Stern H.S., and Rubin D.B. Bayesian Data Analysis (1995), Chapman and Hall, London
29. Goedefroit, S., 1998. A l'ouest de Madagascar: les Sakalava de Menabe. Karthala/ORSTOM, Paris.
30. Goodman S.M., and Benstead J.P. The Natural History of Madagascar (2003), The University of Chicago Press, Chicago and London
31. Goodman S.J., Tamate H.B., Wilson R., Nagata J., Tatsuzawa S., Swanson G.M., Pemberton J.M., and McCullough D.R. Bottlenecks, drift and differentiation: the population structure and demographic history of sika deer (Cervus nippon) in the Japanese archipelago. Molecular Ecology 10 (2001) 1357-1370
32. Goossens B., Chikhi L., Taberlet P., Waits L.P., and Allainé D. Microsatellite analysis of genetic variation among Alpine marmot populations in the French Alps. Molecular Ecology 10 (2001) 41-52
33. Goossens B., Chikhi L., Ancrenaz M., Lackman-Ancrenaz I., Andau P., and Bruford M.W. Genetic signature of anthropogenic population collapse in orang-utans. PloS Biology 4 (2006) 285-291
34. Guschanski K., Olivieri G., Funk S.M., and Radespiel U. MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis. Conservation Genetics 8 (2007) 809-821
35. Hapke A., Eberle M., and Zischler H. Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.). Molecular Ecology Notes 3 (2003) 205-208
36. Jekielek J., and Strobeck C. Characterization of polymorphic brown lemur (Eulemur fulvus) microsatellite loci and their amplification in the family Lemuridae. Molecular Ecology 8 (1999) 901-903
37. Joyce D.A., and Pullin A.S. Conservation implications of the distribution of genetic diversity at different scales: a case study using the marsh fritillary butterfly (Euphydryas aurinia). Biological Conservation 114 (2003) 453-461
38. Kappeler P.M., Rasoloarison R.M., Razafimanantsoa L., Walter L., and Roos C. Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Report 71 (2005) 3-26
39. Keller I., Excoffier L., and Largiadèr C.R. Estimation of effective population size and detection of a recent population decline coinciding with habitat fragmentation in a ground beetle. Journal of Evolutionary Biology 18 (2005) 90-100
40. Kent R.K. Early Kingdoms of Madagascar 1500-1700 (1970), Holt, Rinehart, Winston, New York
41. Knaepkens G., Bervoets L., Verheyen E., and Eens M. Relationship between population size and genetic diversity in endangered populations of the European bullhead (Cottus gobio): implications for conservation. Biological Conservation 115 (2004) 403-410
42. Louis E.E., Coles M.S., Andriantompohavana R., Sommer J.A., Engberg S.E., Zaonarivelo J.R., Mayor M.I., and Brenneman R.A. Revision of the mouse lemurs (Microcebus) of eastern Madagascar. International Journal of Primatology 27 (2006) 347-389
43. Maniatis T., Fritsch E.F., and Sambrook J. Molecular Cloning: a Laboratory Manual (1982), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
44. Matsumoto K., and Burney D.A. Late Holocene environmental changes at Lake Mitsinjo, northwestern Madagascar. The Holocene 4 (1994) 16-24
45. Merenlender, 1993. The Effects of Sociality on the Demography and Genetic Strucuture of Lemur fulvus rufus (polygamous) and Lemur rubiventer (monogamous) and the Conservation Implications, University of Rochester, Rochester.
46. Mittermeier, R.A., Konstant, W.R., Hawkins, F., Louis, E.E., Langrand, O., Ratsimbazafy, J., Rasoloarison, R., Ganzhorn, J.U., Rajaobelina, S., Tattersall, I., Meyers, D.M., 2006. Lemurs of Madagascar, second ed. Conservation International Tropical Field Guide Series.
47. Müller A.E., and Thalmann U. Origin and evolution of primate social organisation: a reconstruction. Biological Reviews 75 (2000) 405-435
48. Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., and Kent J. Biodiversity hotspots for conservation priorities. Nature 403 (2000) 853-858
49. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 (1978) 583-590
50. Nicoll M.E. Forests outside protected areas. In: Goodman S.M., and Benstead J.P. (Eds). The Natural History of Madagascar (2003), The University of Chicago Press, Chicago and London 1432-1437
51. Nyström V., Angerbjörn A., and Dalén L. Genetic consequences of a demographic bottleneck in the Scandinavian arctic fox. OIKOS 114 (2006) 84-94
52. Olivieri G.L., Craul M., and Radespiel U. Inventaire des lémuriens dans 15 fragments de forêt de la province de Mahajanga. Lemur News 10 (2005) 11-16
53. Olivieri G.L., Zimmermann E., Randrianambinina B., Rasoloharijaona S., Rakotondravony D., Guschanski K., and Radespiel U. The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution 43 (2007) 309-327
54. Pastorini J., Martin R.D., Ehresmann P., Zimmermann E., and Forstner M.R. Molecular phylogeny of the lemur family Cheirogaleidae (primates) based on mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 19 (2001) 45-56
55. Piry S., Luikart G., and Cornuet J.-M. BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90 (1999) 502-503
56. Pritchard J.K., Stephens M., and Donnelly P. Inference of population structure using multilocus genotype data. Genetics 155 (2000) 945-959
57. Radespiel U. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In: Gould L., and Sauther M.L. (Eds). Lemurs. Ecology and adaptation (2006), Springer, New York 211-233
58. Radespiel U., Funk S.M., Zimmermann E., and Bruford M.W. Isolation and characterization of microsatellite loci in the grey mouse lemur (Microcebus murinus) and their amplification in the family Cheirogaleidae. Molecular Ecology Notes 1 (2001) 16-18
59. Radespiel U., Lutermann H., Schmelting B., Bruford M.W., and Zimmermann E. Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Animal Behaviour 65 (2003) 709-719
60. Radimilahy M. Mahilaka, an eleventh- to fourtheenth-century Islamic port. In: Goodman S.M., and Patterson B.D. (Eds). Natural Change and Human Impact in Madagascar (1997), Smithsonian Institute Press, Washington, DC 342-363
61. Radimilahy, M., 1998. Mahilaka: Archeological Studies of an Early Port in Northwestern Madagascar, Studies in African archeology. Societas Archeologica Uppsaliensis and Department of Archeology and Ancient History, Uppsala.
62. Rakotondravony, R., 2007. Biogéographie de Microcebus ravelobensis et de M. murinus dans le Parc National d'Ankarafantsika, Madagascar, Thèse de Doctorat, Université d'Antananarivo.
63. Rasoloarison R.M., Goodman S.M., and Ganzhorn J.U. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology 21 (2000) 963-1019
64. Rousset F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145 (1997) 1219-1228
65. Schad J., Sommer S., and Ganzhorn J.U. MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conservation Genetics 5 (2004) 299-309
66. Schmid J., and Kappeler P.M. Sympatric mouse lemurs (Microcebus spp.) in Western Madagascar. Folia Primatologica 63 (1994) 162-170
67. Scott D.M., Brown D., Mahood S., Denton B., Silburn A., and Rakotondraparany F. The impacts of forest clearance on lizard, small mammal and bird communities in the arid spiny forest, southern Madagascar. Biological Conservation 127 (2006) 72-87
68. Seutin G., White B.N., and Boag P.T. Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 69 (1991) 82-90
69. Smith P.S. Deforestation, fragmentation, and reserve design in western Madagascar. In: Laurance W.F., and Bierregaard R.O. (Eds). Tropical Forest Remnants: Ecology, Managment, and Conservation of Fragmented Communities (1997), The University of Chicago Press, Chicago and London 415-441
70. Storz J.F., and Beaumont M.A. Testing for genetic evidence of population expansion and contraction: An empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56 (2002) 154-166
71. Telles M.P.C., Diniz-Filho J.A.F., Bastos R.P., Soares T.N., Guimarães L.D., and Lima L.P. Landscape genetics of Physalaemus cuvieri in Brazilian Cerrado: Correspondence between population structure and patterns of human occupation and habitat loss. Biological Conservation 139 (2007) 37-46
72. Turner T.F., Dowling T.E., Broughton R.E., and Gold J.R. Variable microsatellite markers amplify across divergent lineages of cyprinid fishes (subfamily Leusicinae). Conservation Genetics 5 (2004) 279-281
73. Vitalis R., and Couvet D. ESTIM 1.0: a computer program to infer population parameters from one- and two-locus gene identity probabilities. Molecular Ecology Notes 1 (2001) 354-356
74. von Segesser F., Menard N., Gaci B., and Martin R.D. Genetic differentiation within and between isolated Algerian subpopulations of Barbary macaques (Macaca sylvanus): evidence from microsatellites. Molecular Ecology 8 (1999) 433-442
75. Wakeley J. Nonequilibrium migration in Human history. Genetics 153 (1999) 1863-1871
76. Wakeley J., and Aliacar N. Gene genealogies in a metapopulation. Genetics 159 (2001) 893-905
77. Weir B.S. Inferences about linkage disequilibrium. Biometrics 35 (1979) 235-254
78. Weir B.S., and Cockerham C.C. Estimating F-Statistics for the analysis of population-structure. Evolution 38 (1984) 1358-1370
79. Wimmer B., Tautz D., and Kappeler P.M. The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behavioural Ecology and Sociobiology 52 (2002) 166-175
80. Wright H.T., and Rakotoarisoa J.A. The rise of Malagasy societies: New developments in the archaeology of Madagascar. In: Goodman S.M., and Benstead J.P. (Eds). The Natural History of Madagascar (2003), The University of Chicago Press, Chicago 112-119
81. Yoder A.D., and Nowak M.D. Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annual Review of Ecology Evolution and Systematics 37 (2006) 405-431
82. Yoder A.D., Rasoloarison R.M., Goodman S.M., Irwin J.A., Atsalis S., Ravosa M.J., and Ganzhorn J.U. Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). PNAS 97 (2000) 11325-11330
83. Zimmermann E., Cepok S., Rakotoarison N., Zietemann V., and Radespiel U. Sympatric mouse lemurs in north-west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatologica 69 (1998) 106-114