Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus)

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Chaves, Paulo B ^a,e   Alvarenga, Clara S ^a   de Possamai, Carla B ^a   Dias, Luiz G ^b   Boubli, Jean P ^c   Strier, Karen B ^d   Mendes, Sérgio L ^a   Fagundes, Valéria ^a  

^a FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^b Instituto Biotrópicos de Pesquisa em Vida Silvestre Diamantina   (Brazil)

^c WILDLIFE CONSERVATION SOCIETY   (Brazil)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL CELL; ARTICLE; BAYES THEOREM; BRACHYTELES; CONTROLLED STUDY; DNA DETERMINATION; ENDANGERED SPECIES; GENETIC VARIABILITY; HAPLOTYPE; HOLOCENE; MATHEMATICAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; PLEISTOCENE; POPULATION DISPERSAL; POPULATION DYNAMICS; POPULATION GROWTH; POPULATION SIZE; POPULATION STRUCTURE; PRIMATE; SPECIES CONSERVATION; ANIMAL; BRAZIL; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; PLATYRRHINI; POPULATION DENSITY; POPULATION GENETICS;

BRACHYTELES ARACHNOIDES; BRACHYTELES HYPOXANTHUS; PLATYRRHINI; PRIMATES;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; BRAZIL; ENDANGERED SPECIES; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; HAPLOTYPES; PLATYRRHINI; POPULATION DENSITY; POPULATION DYNAMICS;

EID: 79958036391     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020722     Document Type: Article

References (98)

1. Sugg DW, Chesser RK, Dobson FS, Hoogland JL, (1996) Population genetics meets behavioral ecology. Trends Ecol Evol 11: 338-342.
2. Di Fiore A, (2003) Molecular genetic approaches to the study of primate behavior, social organization, and reproduction. Yearb Phys Anthropol 46: 62-99.
3. Vigilant L, Guschanski K, (2009) Using genetics to understand the dynamics of wild primate populations. Primates 50: 105-120.
4. Avise JC, (2000) Phylogeography: the history and formation of species. Cambridge Harvard University Press.
5. Cowlishaw G, Dunbar R, (2000) Primate Conservation Biology. Chicago University of Chicago Press.
6. Pope TR, (1992) The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus). Evolution 46: 1112-1128.
7. Goossens B, Chikhi L, Ancrenaz M, Lackman-Ancrenaz I, Andau P, et al. (2006) Genetic signature of anthropogenic population collapse in orang-utans. PLoS Biol 4: 285-291.
8. Dietz JM, Baker AJ, Ballou JD, (2000) Demographic evidence of inbreeding depression in wild golden lion tamarins. In: Young A, Clark G, editors. Genetics, demography, and viability of fragmented populations Cambridge Cambridge University Press pp. 203-211.
9. Pope TR, (1996) Socioecology, population fragmentation, and patterns of genetic loss in endangered primates. In: Avise JC, Hamrick JL, editors. Conservation Genetics: Case Histories from Nature New York Chapman and Hall pp. 119-159.
10. Pope TR, (1998) Effects of demographic change on group kin structure and gene dynamics of populations of red howling monkeys. J Mammal 79: 692-712.
11. Stockwell CA, Hendry AP, Kinnison MT, (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18: 94-101.
12. Carnaval AC, Moritz C, (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35: 1187-1201.
13. Costa LP, (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30: 71-86.
14. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C, (2009) Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot. Science 323: 785-789.
15. Thomé MTC, Zamudio KR, Giovanelli JGR, Haddad CFB, Baldissera FA, et al. (2010) Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic Forest. Mol Phylogen Evol 55: 1018-1031.
16. Behling H, (2002) South and southeast Brazilian grasslands during Late Quaternary times: a synthesis. Palaeogeogr Palaeoclimatol Palaeoecol 177: 19-27.
17. Brown KS, (2005) Geological, evolutionary, and ecological bases of the diversification of Neotropical butterflies: implications for conservation. In: Berminhgan E, Dick CW, Moritz C, editors. Tropical Rainforest: Past, Present and Future Chicago University of Chicago Press pp. 166-201.
18. Ledru MP, Rousseau DD, Cruz FW, Riccomini C, Karmann I, et al. (2005) Paleoclimate changes during the last 100,000 yr from a record in the Brazilian Atlantic rainforest region and interhemispheric comparison. Quatern Res 64: 444-450.
19. Costa LP, Leite YLR, da Fonseca GAB, da Fonseca MT, (2000) Biogeography of South American forest mammals: Endemism and diversity in the Atlantic Forest. Biotropica 32: 872-881.
20. Aguirre AC, (1971) O mono Brachyteles arachnoides (E. Geoffroy). Situação atual da espécie no Brasil. An Acad Bras Cienc 1: 1-53.
21. Lemos de Sá RM, Glander KE, (1993) Capture techniques and morphometrics for the woolly spider monkey, or muriqui (Brachyteles arachnoides, Geoffroy, E. 1806). Am J Primatol 29: 145-153.
22. Fleagle JG, (1999) Primate adaptation and evolution, second edition. San Diego Academic Press.
23. Vieira CC, (1944) Os símios do Estado de São Paulo, Pap Avulsos Zool 4: 1-31.
24. Groves CP, (2005) Order primates. In: Wilson DE, Reeder DM, editors. Mammal species of the World: A taxonomic and geographic reference, third edition Maryland Johns Hopkins University Press pp. 111-184.
25. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J, (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
26. Galindo-Leal C, Câmara IG, (2003) Atlantic Forest hotspot status: an overview. In: Galindo-Leal C, Câmara IG, editors. The Atlantic Forest of South America: biodiversity status, threats, and outlook Washington DC Island Press pp. 360-371.
27. Mendes SL, Melo FR, Boubli JP, Dias LG, Strier KB, et al. (2005) Directives for the conservation of the northern muriqui, Brachyteles hypoxanthus (Primates, Atelidae). Neotrop Primates 13: 7-18.
28. Melnick DJ, Hoelzer GA, (1992) Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. Int J Primatol 13: 379-393.
29. Storz JF, (1999) Genetic consequences of mammalian social structure. J Mammal 80: 553-569.
30. Strier KB, Boubli JR, Possamai CB, Mendes SL, (2006) Population demography of northern muriquis (Brachyteles hypoxanthus) at the Estacao Biologica de Caratinga/Reserva Particular do Patrimonio Natural-Feliciano Miguel Abdala, Minas Gerais, Brazil. Am J Phys Anthropol 130: 227-237.
31. Chesser RK, (1991) Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129: 573-583.
32. Strier KB, (2008) The effects of kin on primate life histories. Annu Rev Anthropol 37: 21-36.
33. Frankham R, (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10: 1500-1508.
34. Strier KB, (2000) Population viabilities and conservation implications for muriquis (Brachyteles arachnoides) in Brazil's Atlantic Forest. Biotropica 32: 903-913.
35. Mendes SL, de Oliveira MM, Mittermeier RA, Rylands AB, (2008) Brachyteles hypoxanthus. 2008 IUCN Red List of Threatened Species, Version 2010.3. Available: http://www.iucnredlist.org. Accessed 2010 Sep 12.
36. Collins AC, Dubach JM, (2000) Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA variation. Int J Primatol 21: 381-420.
37. Fagundes V, Paes MF, Chaves PB, Mendes SL, Possamai CD, et al. (2008) Genetic structure in two northern muriqui populations (Brachyteles hypoxanthus, Primates, Atelidae) as inferred from fecal DNA. Genet Mol Biol 31: 166-171.
38. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
39. Hall TA, (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
40. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
41. Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
42. Nei M, (1987) Molecular evolutionary genetics. New York Columbia University Press.
43. Posada D, (2008) jModelTest: Phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
44. Akaike H, (1974) A new look at the statistical identification model. IEEE Transactions on Automatic Control 19: 716-723.
45. Colwell RK, (2006) ESTIMATES: Statistical estimation of species richness and shared species from samples, Version 8. Available: <purl.oclc.org/estimates>. Accessed 2010 Feb 5.
46. Peters JL, Zhuravlev YN, Fefelov I, Humphries EM, Omland KE, (2008) Multilocus phylogeography of a Holarctic duck: Colonization of North America from Eurasia by gadwall (Anas strepera). Evolution 62: 1469-1483.
47. Tamura K, Nei M, (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
48. Carvajal-Rodriguez A, de Una-Alvarez J, Rolan-Alvarez E, (2009) A new multitest correction (SGoF) that increases its statistical power when increasing the number of tests. Bmc Bioinformatics 10.
49. Takahata N, Palumbi SR, (1985) Extranuclear differentiation and gene flow in the finite island model. Genetics 109: 441-457.
50. Mantel N, (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27: 209-220.
51. Smouse PE, Long JC, Sokal RR, (1986) Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35: 627-632.
52. Jensen JL, Bohonak AJ, Kelley ST, (2005) Isolation by distance, web service. BMC Genet 6: 13.
53. Bandelt HJ, Forster P, Rohl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
54. Fu YX, (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.53.
55. Fu YX, Li WH, (1993) Statistical tests of neutrality of mutations. Genetics 133: 693-709.
56. Ramos-Onsins SE, Rozas J, (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092-2100.
57. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R, (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
58. Ramirez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A, (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179: 555-567.
59. Kuhner MK, (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22: 768-770.
60. Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
61. Cornuet JM, Ravigne V, Estoup A, (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). Bmc Bioinformatics 11.
62. Beerli P, (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13: 827-836.
63. Beerli P, (2008) Migrate version 3.0- a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Available: http://popgen.scs.edu/migrate.html. Accessed 2009 Oct 20.
64. Rambaut A, Drummond AJ, (2007) Tracer v1.4. Available: http://beast.bio.ed.ac.uk/Tracer. Acessed 2009 Nov 6.
65. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. Vienna, Austria. Available: http://www.R-project.org.
66. Schrago CG, Russo CAM, (2003) Timing the origin of New World monkeys. Mol Biol Evol 20: 1620-1625.
67. Poux C, Chevret P, Huchon D, de Jong WW, Douzery EJP, (2006) Arrival and diversification of caviomorph rodents and platyrrhine primates in South America. Syst Biol 55: 228-244.
68. Hodgson JA, Sterner KN, Matthews LJ, Burrell AS, Jani RA, et al. (2009) Successive radiations, not stasis, in the South American primate fauna. Proc Natl Acad Sci U S A 106: 5534-5539.
69. Galtier N, Jobson RW, Nabholz B, Glemin S, Blier PU, (2009) Mitochondrial whims: metabolic rate, longevity and the rate of molecular evolution. Biol Lett 5: 413-416.
70. Collins AC, Dubach JM, (2000) Biogeographic and ecological forces responsible for speciation in Ateles. Int J Primatol 21: 421-444.
71. Lessios HA, (2008) The Great American Schism: Divergence of Marine Organisms After the Rise of the Central American Isthmus. Annu Rev Ecol Evol Syst 39: 63-91.
72. Posada D, Crandall KA, (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16: 37-45.
73. Melo FR, Dias LG, (2005) Muriqui populations reported in the literature over the last 40 years. Neotrop Primates 13: 19-24.
74. Ascunce MS, Hasson E, Mulligan CJ, Mudry MD, (2007) Mitochondrial sequence diversity of the southernmost extant New World monkey, Alouatta caraya. Mol Phylogen Evol 43: 202-215.
75. Di Fiore A, (2009) Genetic approaches to the study of dispersal and kinship in New World primates. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, editors. South American primates: comparative perspectives in the study of behavior, ecology, and conservation New York Springer Science+Business Media pp. 211-250.
76. Liu Z, Ren B, Wei F, Long Y, Hao Y, et al. (2007) Phylogeography and population structure of the Yunnan snub-nosed monkey (Rhinopithecus bieti) inferred from mitochondrial control region DNA sequence analysis. Mol Ecol 16: 3334-3349.
77. Deinard AS, Kidd K, (2000) Identifying conservation units within captive chimpanzee populations. Am J Phys Anthropol 111: 25-44.
78. Vigilant L, Bradley BJ, (2004) Genetic variation in gorillas. Am J Primatol 64: 161-172.
79. Jalil MF, Cable J, Inyor JS, Lackman-Ancrenaz I, Ancrenaz M, et al. (2008) Riverine effects on mitochondrial structure of Bornean orang-utans (Pongo pygmaeus) at two spatial scales. Mol Ecol 17: 2898-2909.
80. Pope TR, (1998) Genetic variation in remnant populations of the woolly spider monkey (Brachyteles arachnoides). Int J Primatol 19: 95-109.
81. Rogers AR, (1988) Three components of genetic drift in subdivided populations. Am J Phys Anthropol 77: 435-449.
82. Valle CMC, Santos IB, Alves MC, Pinto CA, Mittermeier RA, (1984) Preliminary observations on the behavior of the monkey (Brachyteles arachnoides) in a natural environment (Fazenda Montes Claros, Municipio de Caratinga, Minas Gerais, Brazil). In: de Mello MT, editors. A Primatologia no Brasil Brasilia Sociedade Brasileira de Primatologia pp. 271-283.
83. Hutchison DW, Templeton AR, (1999) Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53: 1898-1914.
84. Brito D, Grelle CEV, (2006) Estimating minimum area of suitable habitat and viable population size for the northern muriqui (Brachyteles hypoxanthus). Biodivers Conserv 15: 4197-4210.
85. Brito D, Grelle CEV, Boubli JP, (2008) Is the Atlantic Forest protected area network efficient in maintaining viable populations of Brachyteles hypoxanthus? Biodivers Conserv 17: 3255-3268.
86. Storz JF, Ramakrishnan U, Alberts SC, (2002) Genetic effective size of a wild primate population: Influence of current and historical demography. Evolution 56: 817-829.
87. Wegmann D, Excoffier L, (2010) Bayesian Inference of the Demographic History of Chimpanzees. Mol Biol Evol 27: 1425-1435.
88. Pakendorf B, Stoneking M, (2005) Mitochondrial DNA and human evolution. Annu Rev Genomics Hum Genet 6: 165-183.
89. Rooney AP, Honeycutt RL, Derr JN, (2001) Historical population size change of bowhead whales inferred from DNA sequence polymorphism data. Evolution 55: 1678-1685.
90. Tchaicka L, Eizirik E, De Oliveira TG, Candido JF, Freitas TRO, (2007) Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Mol Ecol 16: 819-838.
91. Strier KB, (1999) The atelines. In: Dolhinow P, Fuentes A, editors. The nonhuman primates California Mayfield Publishing Company pp. 109-114.
92. Nishimura A, (2003) Reproductive parameters of wild female Lagothrix lagotricha. Int J Primatol 24: 707-722.
93. Galtier N, Nabholz B, Glemin S, Hurst GDD, (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18: 4541-4550.
94. Moritz C, (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9: 373-375.
95. Traill LW, Brook BW, Frankham RR, Bradshaw CJA, (2010) Pragmatic population viability targets in a rapidly changing world. Biological Conservation 143: 28-34.
96. Scott JM, Goble DD, Haines AM, Wiens JA, Neel MC, (2010) Conservation-reliant species and the future of conservation. Conservation Letters 3: 91-97.
97. Moritz C, (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130: 217-228.
98. Instituto Chico Mendes Para a Conservação da Biodiversidade (2010) Portaria N° 87, de 27 de agosto de 2010. Diário Oficial da União 02/09/2010: 100.