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Genetic Diversity and Population History of a Critically Endangered Primate, the Northern Muriqui (Brachyteles hypoxanthus)

By Paulo B. Chaves, Clara S. Alvarenga, Carla de B. Possamai, Luiz G. Dias, Jean P. Boubli, Karen B. Strier, Sérgio L. Mendes and Valéria Fagundes

Abstract

Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (ΦST = 0.49, ΦCT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3108597
Provided by: PubMed Central

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Citations

  1. (2003). A
  2. A (2009) Genetic approaches to the study of dispersal and kinship in New World primates.
  3. (1974). A new look at the statistical identification model.
  4. (2009). A new multitest correction (SGoF) that increases its statistical power when increasing the number of tests.
  5. (2005). Arlequin (version 3.0): An integrated software package for population genetics data analysis.
  6. (2006). Arrival and diversification of caviomorph rodents and platyrrhine primates in South America.
  7. (2010). Bayesian Inference of the Demographic History of Chimpanzees.
  8. (2000). Biodiversity hotspots for conservation priorities.
  9. (1999). BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.
  10. (2000). Biogeographic and ecological forces responsible for speciation in Ateles.
  11. (2000). Biogeography of South American forest mammals: Endemism and diversity in the Atlantic Forest.
  12. (2008). Brachyteles hypoxanthus.
  13. Ca ˆmara IG (2003) Atlantic Forest hotspot status: an overview. In: Galindo-Leal C, Ca ˆmara IG, eds. The Atlantic Forest of South America: biodiversity status, threats, and outlook. Washington DC:
  14. (1993). Capture techniques and morphometrics for the woolly spider monkey, or muriqui (Brachyteles arachnoides,
  15. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
  16. (1999). Conservation units and translocations: strategies for conserving evolutionary processes.
  17. (2010). Conservationreliant species and the future of conservation.
  18. (2003). Contemporary evolution meets conservation biology.
  19. (2010). Core Team
  20. (1999). Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability.
  21. (1994). Defining evolutionarily significant units for conservation.
  22. (2000). Demographic evidence of inbreeding depression in wild golden lion tamarins. In: Young A,
  23. (1967). Detection of disease clustering and a generalized regression approach.
  24. (1992). Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation.
  25. (2005). Directives for the conservation of the northern muriqui, Brachyteles hypoxanthus (Primates,
  26. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods.
  27. (2004). Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations.
  28. (1998). Effects of demographic change on group kin structure and gene dynamics of populations of red howling monkeys.
  29. (2006). ESTIMATES: Statistical estimation of species richness and shared species from samples,
  30. (2006). Estimating minimum area of suitable habitat and viable population size for the northern muriqui (Brachyteles hypoxanthus).
  31. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.
  32. Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0).
  33. (1985). Extranuclear differentiation and gene flow in the finite island model.
  34. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
  35. (1999). Genetic consequences of mammalian social structure.
  36. (2006). Genetic signature of anthropogenic population collapse in orang-utans.
  37. (2008). Genetic structure in two northern muriqui populations (Brachyteles hypoxanthus, Primates, Atelidae) as inferred from fecal DNA.
  38. (2004). Genetic variation in gorillas.
  39. (1998). Genetic variation in remnant populations of the woolly spider monkey (Brachyteles arachnoides).
  40. (2005). Geological, evolutionary, and ecological bases of the diversification of Neotropical butterflies: implications for conservation. In: Berminhgan
  41. (2008). Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest.
  42. (2001). Historical population size change of bowhead whales inferred from DNA sequence polymorphism data.
  43. (2000). Identifying conservation units within captive chimpanzee populations.
  44. (1991). Influence of gene flow and breeding tactics on gene diversity within populations.
  45. (2011). Instituto Chico Mendes Para a Conservac ¸a ˜o da Biodiversidade (2010) Portaria Nu 87, de 27 de agosto de 2010. Dia ´rio Oficial da Unia ˜o 02/09/2010: 100.
  46. (2001). Intraspecific gene genealogies: trees grafting into networks.
  47. (2008). Is the Atlantic Forest protected area network efficient in maintaining viable populations of Brachyteles hypoxanthus?
  48. (2005). Isolation by distance, web service.
  49. (2008). jModelTest: Phylogenetic model averaging.
  50. (2006). LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters.
  51. (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
  52. (2005). Mitochondrial DNA and human evolution.
  53. (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal.
  54. (2007). Mitochondrial sequence diversity of the southernmost extant New World monkey, Alouatta caraya.
  55. (2009). Mitochondrial whims: metabolic rate, longevity and the rate of molecular evolution.
  56. (1987). Molecular evolutionary genetics.
  57. (2008). Multilocus phylogeography of a Holarctic duck: Colonization of North America from Eurasia by gadwall (Anas strepera).
  58. (1986). Multiple regression and correlation extensions of the mantel test of matrix correspondence.
  59. (2005). Muriqui populations reported in the literature over the last 40 years.
  60. (2008). Navarro A
  61. (1971). O mono Brachyteles arachnoides
  62. (2005). Order primates. In:
  63. (1944). Os sı ´mios do Estado de Sa ˜o Paulo,
  64. (2005). Paleoclimate changes during the last 100,000 yr from a record in the Brazilian Atlantic rainforest region and interhemispheric comparison.
  65. (2000). Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA variation.
  66. (2007). Phylogeography and population history of the crab-eating fox (Cerdocyon thous).
  67. (2007). Phylogeography and population structure of the Yunnan snub-nosed monkey (Rhinopithecus bieti) inferred from mitochondrial control region DNA sequence analysis.
  68. (2010). Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic Forest.
  69. (2000). Phylogeography: the history and formation of species. Cambridge:
  70. (2006). Population demography of northern muriquis (Brachyteles hypoxanthus) at the Estacao Biologica de Caratinga/Reserva Particular do Patrimonio Natural-Feliciano Miguel Abdala,
  71. (1996). Population genetics meets behavioral ecology.
  72. (2000). Population viabilities and conservation implications for muriquis (Brachyteles arachnoides) in Brazil’s Atlantic Forest.
  73. (2010). Pragmatic population viability targets in a rapidly changing world.
  74. (1984). Preliminary observations on the behavior of the monkey (Brachyteles arachnoides) in a natural environment (Fazenda Montes Claros, Municipio de Caratinga,
  75. (2000). Primate Conservation Biology.
  76. (2007). Rambaut A
  77. (1996). Relationship of genetic variation to population size in wildlife.
  78. (2003). Reproductive parameters of wild female Lagothrix lagotricha.
  79. (2008). Riverine effects on mitochondrial structure of Bornean orang-utans (Pongo pygmaeus) at two spatial scales.
  80. (1999). Rohl A
  81. (1996). Socioecology, population fragmentation, and patterns of genetic loss in endangered primates.
  82. (2002). South and southeast Brazilian grasslands during Late Quaternary times: a synthesis. Palaeogeogr Palaeoclimatol Palaeoecol 177:
  83. (2009). Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot.
  84. (2002). Statistical properties of new neutrality tests against population growth.
  85. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection.
  86. (1993). Statistical tests of neutrality of mutations.
  87. (2009). Successive radiations, not stasis, in the South American primate fauna.
  88. (1999). The atelines. In: Dolhinow
  89. (2008). The effects of kin on primate life histories.
  90. (2008). The Great American Schism: Divergence of Marine Organisms After the Rise of the Central American Isthmus.
  91. (2003). The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals.
  92. (1992). The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus).
  93. (1988). Three components of genetic drift in subdivided populations.
  94. (2003). Timing the origin of New World monkeys.
  95. (2009). Using genetics to understand the dynamics of wild primate populations.