International Journal of Primatology

, Volume 21, Issue 3, pp 381–420

Phylogenetic Relationships of Spider Monkeys (Ateles) Based on Mitochondrial DNA Variation

  • A. C. Collins
  • J. M. Dubach
Article

Abstract

Our goal was to determine phylogenetic relationships among geographically and taxonomically distinct haplotypes of spider monkeys (Ateles) based on DNA sequence variation for the mitochondrial DNA control region and cytochrome c oxidase subunit II gene. We obtained samples from most previously recognized subspecies of Ateles, ranging from Central America throughout the Amazon Basin, to determine phylogenetic relationships among racially recognized groups. Comparison of DNA sequences using both parsimony analysis and genetic distance analysis produced phylogenetic relationships that were very similar for each genetic region. We analyzed the phylograms produced, along with associated bootstrap support, confidence probabilities, and genetic distances between taxonomic groups, to identify four monophyletic species of Ateles: Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; A. belzebuth in the southern Amazon Basin; A. hybridus, located primarily along the Magdalena River valley of Colombia; and A. geoffroyi, which includes two former species: A. geoffroyi and A. fusciceps. This arrangement is contradictory to long-held taxonomies of Ateles based on pelage variation and is similar to a recent analysis based on craniodental variation. Results of this investigation suggest patterns of gene flow, evolutionary relationships, and speciation patterns that are more plausible than previous pelage-based taxonomies, which required seemingly impossible patterns of gene flow. Conservation efforts aimed at protecting Ateles, one of the Neotropics most endangered genera, will also benefit from the findings presented in this paper.

phylogenetics taxonomy systematic Ateles Cebidae 

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REFERENCES

  1. Adkins, R. M., and Honeycutt, R. L. (1994). Evolution of the primate cytochrome c oxidase subunit II gene. J. Mol. Evol. 38: 215-231.Google Scholar
  2. Alvard, M. S. (1994). The sustainability of primate hunting in the Neotropics: Data from two native communities. Am. J. Phys. Anthropol. (Suppl.) 18(94): 49.Google Scholar
  3. Alvard, M. (1995). Shotguns and sustainable hunting in the Neotropics, Oryx 29: 58-65.Google Scholar
  4. Aquino, R., and Encarnacion, F. (1994). Primates of Peru. Primate Rep. 40: 1-127.Google Scholar
  5. Ashley, M. V., and Vaughn, J. L. (1995). Owl monkeys (Aotus) are highly divergent in mitochondrial cytochrome c oxidase (COII) sequences. Int. J. Primatol. 16: 793-806.Google Scholar
  6. Bailey, W. J., Fitch, D. H., Tagle, D. A., Czelusniak, J., Slightom, J. L., and Goodman, M. (1991). Molecular evolution of the psi, nu-globin gene locus: Gibbon phylogeny and the hominoid slowdown. Mol. Biol. Evol. 8: 155-184.Google Scholar
  7. Bodmer, R. E., Puertas, P. E., and Fang, T. G. (1994). The urgency of finding new directions for primate conservation in western Amazonia. Neotrop. Primates 2: 1-3.Google Scholar
  8. Brown, K. S. (1987). Conclusions, synthesis, and alternative hypotheses. In Whitmore, T. C., and Prance, G. T. (eds.), Biogeography and Ouaternary History in Tropical America, Clarendon Press, Oxford, pp. 175-210.Google Scholar
  9. Bush, M. B. (1994). Amazonian speciation:Anecessarily complex model, J. Biogeogr. 21: 5-17.Google Scholar
  10. Campbell, R. C. (1989). Statistics for Biologists, Cambridge University Press, Cambridge.Google Scholar
  11. Cant, J. G. H. (1990). Feeding ecology of spider monkeys (Ateles geoffroyi) at Tikal, Guatemala, Hum. Evol. 5: 269-281.Google Scholar
  12. Colinvaux, P. A. (1996). Quartenary environmental history and forest diversity in the Neotropics. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America, University of Chicago Press, Chicago, pp. 359-406.Google Scholar
  13. Collins, A. C. (1999). Species status of the Colombian spider monkey Ateles belzebuth hybridus. Neotrop. Primates Newsl. 7(2): 39-41.Google Scholar
  14. Collins, A. C., and Dubach, J. M. (2000). Biogeographic and ecological forces responsible for speciation in Ateles. Int. J. Primatol. 21: 421-444.Google Scholar
  15. Dahl, J. F. (1986). The status of howler, spider and Capuchin monkey populations in Belize, Central America. Primate Rep. 14: 161.Google Scholar
  16. de Boer, L. E. M., and de Bruijn, M. (1990). Chromosomal distinction between the red-faced and black-faced black spider monkeys (Ateles paniscus paniscus and A. p. chamek). Zoo Biol. 9: 307-316.Google Scholar
  17. Endler, J. A. (1982). Pleistocene forest refuges: Fact or fancy? In Prance, G. T. (ed.), Biological Diversification in the Tropics, Columbia University Press, New York, pp. 641-656.Google Scholar
  18. Estrada, A., and Coates-Estrada, R. (1988). Tropical rain forest conversion and perspectives in the conservation of wild primates (Alouatta and Ateles) in Mexico. Am. J. Primatol. 14: 315-327.Google Scholar
  19. Fedigan, L. M., Fedigan, L., Chapman, C., and Glander, K. E. (1988). Spider monkey home ranges: A comparison of radio telemetry and direct observation. Am. J. Primatol. 16: 19-29.Google Scholar
  20. Felsenstein, J. (1995). Phylogeny Inference Package (PHYLIP) Version 3.572c. Google Scholar
  21. Froehlich, J. W., Supriantna, J., and Froehlich, P. H. (1991). Morphometric analyses of Ateles: Systematic and biogeographic implications. Am. J. Primatol. 25: 1-22.Google Scholar
  22. Garcia, M., Caballin, M. R., Aragones, J., Goday, C., and Egozcue, J. (1975). Banding patterns of the chromosomes of Ateles geoffroyi with description of two cases of pericentric inversion. J. Med. Primatol. 4: 108-113.Google Scholar
  23. Groves, C. P. (1989). A Theory of Human and Primate Evolution, Clarendon Press, Oxford, pp. 127-131.Google Scholar
  24. Haffer, J. (1982). General aspects of the refuge theory. In Prance, G. T. (ed.), Biological Diversification in the Tropics, Columbia University Press, New York, pp. 5-22.Google Scholar
  25. Haffer, J. (1987). Quartenary history of tropical America. In Whitmore, T. C., and Prance, G. T. (eds.), Biogeography and Quaternary History in Tropical America, Clarendon Press, Oxford, pp. 1-18.Google Scholar
  26. Haffer, J. (1997). Alternative models of vertebrate speciation in Amazonia: An overview. Biodivers. Conserv. 6: 451-476.Google Scholar
  27. Harada, M. L., Schneider, H., Schneider, M. P. C., Sampaio, I., Czelusniak, J., and Goodman, M. (1995). DNA evidence of the phylogenetic systematics of New World Monkeys: Support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. Mol. Phylogenet. Evol. 4: 331-349.Google Scholar
  28. Hernandez-Camacho, J., and Cooper, R. W. (1976). The nonhuman primates of Colombia. In Thorington, R. W., and Heltne, P. G. (eds.), Neotropical Primates: Field Studies and Conservation, National Academy of Sciences, Washington, D.C., pp. 35-69.Google Scholar
  29. Hershkovitz, P. (1968). Metachromism or the principle of evolutionary change in mammalian tegumentary colors. Evolution 22: 556-575.Google Scholar
  30. Hershkovitz, P. (1969). The evolution of mammals in southern continents. VI The Recent mammals of the Neotropical region: A zoogeographic and ecological review. Q. Rev. Biol. 44: 1-70.Google Scholar
  31. Hershkovitz, P. (1970). Notes on Tertiary Platyrrhine monkeys and description of a new genus from the Late Miocene of Colombia. Folia Primatol. 12: 1-37.Google Scholar
  32. Hillis, D. M., and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42: 182-192.Google Scholar
  33. Hillis, D. M., and Huselenbeck, J. P. (1992). Signal, noise, and reliability in molecular phylogenetic analysis. J. Hered. 83: 189-195.Google Scholar
  34. Hillis, D. M., Moritz, C., and Mable, B. K. (1996). Molecular Systematics, 2nd ed., Sinauer, Sunderland, Massachusetts, pp. 243-245.Google Scholar
  35. Jacobs, S. C., Larson, A., and Cheverud, J. M. (1995). Phylogenetic relationships and orthogenetic evolution of coat color among tamarins (Genus Saguinus). Syst. Biol. 44: 515-532.Google Scholar
  36. Johns, A. D., and Skorupa, J. P. (1987). Responses of rain-forest primates to habitat disturbance: A review, Int. J. Primatol. 8: 157-191.Google Scholar
  37. Kellogg, R., and Goldman, E. A. (1944). Review on the spider monkeys. Proc. U.S. Mus. Nat. Hist. 96: 1-45.Google Scholar
  38. Kimbel, W. H., and Martin, L. B. (1993). Species and speciation: Conceptual issues and their relevance for primate evolutionary biology. In Kimbel, W. H., and Martin, L. B. (eds.), Species, Species Concepts, and Primate Evolution, Plenum Press, New York.Google Scholar
  39. Kimura, M. (1980). A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol. 16: 111-120.Google Scholar
  40. Kinzey, W. G. (1997). New World Primates: Ecology, Evolution and Behavior. Aldine de Gruyter, New York, pp. 192-199.Google Scholar
  41. Klein, L. L., and Klein, D. B. (1977). Feeding behavior of the Colombian spider monkey. In Clutton-Brock, T. H. (ed.), Primate Ecology, Academic Press, London, pp. 153-185.Google Scholar
  42. Kluge, A. G. (1989). A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 38: 7-25.Google Scholar
  43. Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Paabo, S., Villablanca, F. X., and Wilson, A. C. (1989). Dynamics of mitochondrialDNAevolution in animals: Amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86: 6196-6200.Google Scholar
  44. Konstant, W., Mittermeier, R. A., and Nash, S. D. (1985). Spider monkeys in captivity and in the wild. Primate Conserv. 5: 82-109.Google Scholar
  45. Kumar, S., Tamura, K., and Nei, M. (1993). MEGA: Molecular Evolutionary Genetics Analysis. Vs. 1.02, Pennsylvania State University, University Park, Pennsylvania.Google Scholar
  46. Kunkel, L. M., Heltne, P. G., and Borgaonkar, D. S. (1980). Chromosomal variation and zoogeography in Ateles. Int. J. Primatol. 1: 223-232.Google Scholar
  47. Li, W. H. (1997). Molecular Evolution, Sinnauer, Sunderland, Massachusetts.Google Scholar
  48. Mann, W. (1938). Monkey folk. Natl. Geogr. Mag. 73: 615-655.Google Scholar
  49. Medeiros, M. A., Barroso, R. M. S., Pieczarka, J. C., Nagamachi, C. Y., Ponsa, M., Garcia, M., Garcia, F., and Egozcue, J. (1997). Radiation and speciation of spider monkeys, genus Ateles from the cytogenetic viewpoint. Am. J. Primatol. 42: 167-178.Google Scholar
  50. Meireles, C., Czelusniak, J., Schneider, M. P. C., Chiu, C.-H., Slightom, J. L., Gumucio, D. L., Muniz, J. A. P. C., Brigido, M. C., Ferreira, H. S., and Goodman, M. (1998). Molecular phylogeny of New World Monkeys (Platyrrhini, Atelinae) based on gamma hemoglobin gene sequences [publication information unavailable], GenBank Accession Numbers AF030092, AF030093, AF030094, AF030095, AF030097, AF030098.Google Scholar
  51. Melnick, D. J., and Hoelzer, G. A. (1993). What is mtDNA good for in the study of primate evolution? Evol. Anthropol. 2: 2-10.Google Scholar
  52. Milton, K. (1981). Estimates of reproductive parameters for free-ranging Ateles geoffroyi. Primates 22: 574-579.Google Scholar
  53. Mittermeier, R. A., Kinzey, W. G., and Mast, R. B. (1989). Neotropical primate conservation. J. Hum. Evol. 18: 597-610.Google Scholar
  54. Moore, J. (1993). Inbreeding and outbreeding in primates: What's wrong with ''the dispersing sex''? In Moore, J. (ed.), The Natural History of Inbreeding and Outbreeding, University of Chicago Press, Chicago.Google Scholar
  55. Morain, S. A. (1984). Systematic and Regional Biogeography, Van Nostrand Reinhold, New York. pp. 177-199.Google Scholar
  56. Morin, P. A., Moore, J. J., Chakraborty, R., Jin, L., Goodall, J., and Woodruff, D. S. (1994). Kin selection, social structure, gene flow, and evolution of chimpanzees. Science 265: 1193-1201.Google Scholar
  57. Nei, M. (1996). Phylogenetic analysis in molecular evolutionary genetics. Annu. Rev. Genet. 30: 371-403.Google Scholar
  58. Newland, K. (1994). North American Regional Studbook for South American Spider Monkeys, Sedgwick County Zoological Society, Wichita, Kansas.Google Scholar
  59. Norconck, M. A., Sussman, R. W., and Phillips-Conroy, J. P. (1996). Primates of Guyana shield forests. In Norconck, M. A., Rosenberger, A. L., and Garber, P. A. (eds.), Adaptive Radiations of Neotropical Primates, Plenum Press, New York, pp. 69-83.Google Scholar
  60. Nunes, A. (1995). Status distribution and viability of wild populations of Ateles belzebuth marginatus. Neotrop. Primates 3: 17-18.Google Scholar
  61. Nunes, A. (1998). Diet and feeding ecology of Ateles belzebuth belzebuth at Maraca Ecological Station, Roraima, Brazil. Folia Primatol. 69: 61-76.Google Scholar
  62. Peres, C. A. (1987). Effects of hunting on primate communities of western Brazilian Amazonia. Int. J. Primatol. 8: 492.Google Scholar
  63. Pieczarka, J., Nagamachi, C. Y., and Barroso, R. M. S. (1989). The karyotype of Ateles paniscus paniscus (Cebidae, Primates): 2n = 32. Rev. Bras. Genet. 12: 543-551.Google Scholar
  64. Pingry, K. (1998). North American Regional Studbook for Ateles geoffroyi, Central American Spider Monkey, Chicago Zoological Society, Brookfield, Illinois.Google Scholar
  65. Porter, C. A., Page, S. L., Czelusniak, J., Schneider, H., Schneider, M. P., Sampaio, I., and Goodman, M. (1997). Phylogeny and evolution of selected primates as determined by sequences of the e-globin locus and 5' flanking regions. Int. J. Primatol. 18: 261-295.Google Scholar
  66. Prance, G. T. (1987). Biogeography of Neotropical plants. In Whitmore, T. C., and Prance, G. T. (eds.), Biogeography and Quaternary History in Tropical America, Clarendon Press, Oxford, pp. 46-65.Google Scholar
  67. Raez-Luna, E. F. (1995). Hunting large primates and conservation of the Neotropical rain forests. Oryx 29: 43-47.Google Scholar
  68. Rossan, P. N., and Baerg, D. C. (1977). Laboratory and feral hybridization of Ateles geoffroyi panamensis Kellogg and Goldman, 1944, in Panama. Primates 18: 235-237.Google Scholar
  69. Rowe, N. (1996). The Pictorial Guide to the Living Primates, Pogonias Press, East Hampton, New York, pp. 107-117.Google Scholar
  70. Ruvolo, M. (1994). Molecular evolutionary processes and conflicting gene trees: The hominoid case. Am. J. Phys. Anthropol. 94: 89-113.Google Scholar
  71. Ryder, O. A., and Chemnick, L. G. (1993). Chromosomal and mitochondrial DNA variation in orangutans. J. Hered. 84: 405-409.Google Scholar
  72. Rylands, A. B., Mittermeier, R. A., and Rodriguez-Luna, E. (1997). Conservation of Neotropical primates: Threatened species and an analysis of primate diversity by country and region. Folia Primatol. 68: 134-160.Google Scholar
  73. Sambrook, J., Fritsch, E. T., and Maniatis, T. (1989). Molecular Cloning:ALaboratory Manual, Vols. 1-3, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.Google Scholar
  74. Sampaio, M. I., Schneider, M. P. C., and Schneider, H. (1993). Contribution of genetic distances studies to the taxonomy of Ateles, particularly Ateles paniscus paniscus and Ateles paniscus chamek. Int. J. Primatol. 14: 895-903.Google Scholar
  75. Schneider, H., Schneider, M. P. C., Sampaio, I., Harada, M. L., Stanhope, M., Czelusniak, J., and Goodman, M. (1993). Molecular phylogeny of the New World Monkeys. Mol. Phylogenet. Evol. 2: 225-242.Google Scholar
  76. Shedd, D. H., and Macedonia, J. M. (1991). Metachromism and its phylogenetic implications for the genus Eulemur (Prosimii: Lemuridae). Folia Primatolo. 57: 221-231.Google Scholar
  77. Silva-Lopez, G., Motta-Gill, J., and Hernandez, A. I. (1996). Taxonomic notes on Ateles geoffroyi. Neotrop. Primates 4: 41-44.Google Scholar
  78. Simpson, B. G., and Haffer, J. (1978). Speciation patterns in the Amazonian forest biota. Annu. Rev. Ecol. System. 9: 497-518.Google Scholar
  79. Swofford, D. L. (1998). PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0b1, Smithsonian Institution, Washington, D.C.Google Scholar
  80. Symington, M. M. (1987). Sex ratio and maternal rank in wild spider monkeys: When daughters disperse. Behav. Ecol. Sociobiol. 20: 421-425.Google Scholar
  81. Symington, M. M. (1988). Demography, ranging patterns, and activity budgets of Black spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru. Am. J. Primatol. 15: 45-67.Google Scholar
  82. Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. Int. J. Primatol. 11: 47-61.Google Scholar
  83. Tagliaro, C. H., Schneider, M. P. C., Schneider, H., Sampaio, I. C., and Stanhope, M. J. (1997). Marmoset phylogenetics, conservation perspectives, and evolution of the mtDNA control region. Mol. Biol. Evol. 14: 674-684.Google Scholar
  84. van der Hammen, T. (1982). Paleoecology of tropical South America. In Prance, G. T. (ed.), Biological Diversification in the Tropics, Columbia University Press, New York, pp. 60-65.Google Scholar
  85. van Roosmalen, M. G. M. (1980). Habitat preferences, diet, feeding strategy, and social organization of the Black Spider monkey (Ateles paniscus paniscus) in Surinam, Ph.D. Thesis, University of Wageningen, Netherlands.Google Scholar
  86. Vigilant, L., Pennington, R., Harpending, H., Kocher, T. D., and Wilson, A. C. (1989). Mitochondrial DNA sequences in single hairs from a southern African population. Proc. Natl. Acad. Sci. USA 86: 9350-9354.Google Scholar
  87. Wolfheim, J. H. (1983). Primates of the World: Distribution, Abundance, and Conservation, University of Washington Press, Seattle, pp. 246-256.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • A. C. Collins
    • 1
    • 3
  • J. M. Dubach
    • 4
  1. 1.Department of AnthropologyUniversity of Wisconsin, MadisonWisconsin
  2. 2.Department of Anthropology/SociologyUniversity of Wisconsin College, WaukeshaWisconsin
  3. 3.Department of AnthropologyUniversity of Wisconsin, MilwaukeeWisconsin
  4. 4.Department of Conservation Biology, Ada F. and Daniel L. Rice Conservation Biology and Research CenterBrookfield Zoological InstitutionBrookfield

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