Genetica

, Volume 114, Issue 3, pp 253–267 | Cite as

Description of the Cytochrome c Oxidase Subunit II Gene in Some Genera of New World Monkeys (Primates, Platyrrhini)

  • Marina S. Ascunce
  • Esteban Hasson
  • Marta D. Mudry
Article

Abstract

Nucleotide sequence variation at the mitochondrial cytochrome c oxidase subunit II gene (COII) was analyzed in 27 New World monkey specimens, nine newly reported herein. The study involved comparisons among platyrrhines and also between platyrrhines and catarrhines. The analysis of the frequencies of transitions and transversions at each codon position showed transitional saturation at third codon position. Neighbor-Joining trees obtained from genetic distances estimated by means of Kimura's (1980) two-parameter model showed poor resolution of phylogenetic relationships among platyrrhine genera. Rates of nucleotide substitutions were largely homogeneous except in the genus Saimiri that showed low numbers of unique substitutions suggesting the maintenance of ancestral or plesiomorphic states of platyrrhine mt DNA nucleotide characters probably due to its large population sizes as compared to other platyrrhines.

catarrhines COII gene genetic distances mt DNA platyrrhines saturation substitutional rate 

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References

  1. Adkins, R.M. &; R.L. Honeycutt, 1994. Evolution of the primate cytochrome c oxidase subunit II gene. J. Mol. Evol. 38(3): 512-231.Google Scholar
  2. Adkins, R.M., R.L. Honeycutt &; T.R. Disotell, 1996. Evolution of eutherian cytochrome c oxidase subunit II: heterogeneous rates of protein evolution and altered interaction with cytochrome c. Mol. Biol. Evol. 13(9): 1393-1404.Google Scholar
  3. Ashley, M.V. &; J.L. Vaughn, 1995. Owl monkeys (Aotus) are highly divergent in mitochondrial cytocrhome c oxidase (COII) sequences. Int. J. Primatol. 16(5): 793-806.Google Scholar
  4. Avise, J.C., 1994. Molecular Markers, Natural History, and Evolution, p. 511, edited by Chapman &; Hall, N.Y. and London.Google Scholar
  5. Avise, J.C., J. Arnold, M.R. Ball, E. Bermingham, T. Lamb, J.E. Neigel, C.A. Reeb &; N.C. Saunder, 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann. Rev. Ecol. Syst. 18: 489-522.Google Scholar
  6. Avise, J.C., B.W. Bowen, T. Lamb, A.B. Meylan &; E. Bermingham, 1992. Mitochondrial DNA evolution at a turtle's pace: evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol. Biol. Evol. 9(3): 457-473.Google Scholar
  7. Bailey, W.J., D.H.A. Fitch, D.A. Tagle &; J. Czelusniak, 1991. Molecular evolution of the psi-eta-globin gene locus: gibbon phylogeny and the molecular clock. Mol. Biol. Evol. 8: 155-184.Google Scholar
  8. Boinski, S., 1999. The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol. Anthro. 8(3): 101-113.Google Scholar
  9. Britten, R.J., 1986. Rates of DNA sequence evolution differ between taxonomic groups. Science 231: 1393-1398.Google Scholar
  10. Brown, G.G. &; M.V. Simpson, 1982. Novel features of animal mt DNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc. Natl. Acad. Sci. USA 79: 3246-3250.Google Scholar
  11. Brown, W.M., 1985. The mitochondrial genome of animals, pp 95-130 in Molecular Evolutionary Genetics, edited by R.J. Mac-Intyre. Plenum, N.Y.Google Scholar
  12. Chapman, C.A. &; L.J. Chapman, 1990. Reproductive biology of captive and free-ranging monkeys. Zoo Biol. 9: 1-9.Google Scholar
  13. Collins, A.C. &; J.M. Dubach, 2000. Biogeographic and ecological forces responsible for speciation in Ateles. Int. J. Primatol. 21: 421-444.Google Scholar
  14. Costello, R.K., C. Dickinson, A.L. Rosenberger, S. Boinski &; F.S. Szalay, 1993. Squirrel monkey (Genus Saimiri) taxonomy: a multidisciplinary study of the biology of species, in Species, Species Concepts, and Primate Evolution, edited by W.H. Kimbel and L.B. Martin. Plenum Press, N.Y.Google Scholar
  15. Disotell, T.R., R.L. Honeycutt &; M. Ruvolo, 1992. Mitochondrial DNA phylogeny of the Old-World Monkey tribe Papionini. Mol. Biol. Evol. 9(1): 1-13.Google Scholar
  16. Eisenberg J.F., 1979. Habitat, economy, and society: Some correlations and hypotheses for the neotropical primates, pp. 215-262 in Primate Ecology and Human Origins: Ecological Influences on Social Organization, edited by I.S. Bernstein &; E.O. Smith. Garland STPM Press, N. Y.Google Scholar
  17. Engel, S.R., K.M. Hogan, J.F. Taylor &; S.D. Davis, 1998. Molecular systematics and paleobiogeography of the South American sigmodontine rodents. Mol. Biol. Evol. 15: 35-49.Google Scholar
  18. Fernandez-Duque, E., M. Rotundo &; C. Sloan, 2001. Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco. Am. J. Primatol. 53(3): 99-108.Google Scholar
  19. Figueiredo, W.B., N.M. Carvalho-Filho, H. Schneider &; I. Sampaio, 1998. Mitochondrial DNA sequences and the taxonomic status of Alouatta seniculus populations in northeastern Amazonia. Neotrop. Primates 6(3): 73-77.Google Scholar
  20. Fleagle, J.G., 1998. Primate Adaptation and Evolution, p. 596, edited by Academic Press, California.Google Scholar
  21. Frati, F., C. Simon, J. Sullivan &; D.L. Swoffordd, 1997. Evolution of the mitochondrial cytochrome oxidase II gene in Collembola. J. Mol. Evol. 44: 145-158.Google Scholar
  22. Garber, P.A. &; S.R. Leigh, 1997. Ontogenetic variation in smallbodied New World primates: implications for patterns of reproduction and infant care. Folia Primatol. (Basel) 68(1): 1-22.Google Scholar
  23. Gillespie, J.H., 1991. Neutral allele theories, pp. 261-290 in The Causes of Molecular Evolution, edited by Oxford University Press, N.Y. and Oxford.Google Scholar
  24. Glander, K.E., 1980. Reproduction and population growth in freeranging mantled howling monkeys. Am. J. Phys. Anthropol. 53: 25-36.Google Scholar
  25. Goodman, M., 1985. Rates of molecular evolution: the hominoid slowdown. BioEssays 3: 9-14.Google Scholar
  26. Graur, D. &; W.-H. Li, 2000. Fundamentals of Molecular Evolution, p. 481, edited by A.D. Sinauer. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  27. Groves, C.P., 1992. Primates, pp. 251-261 in Mammal Species of the World: A Taxonomic and Geographic Reference, edited by D.E. Wilson &; D.A.M. Reeder. Smithsonian Institution Press, Washington and London.Google Scholar
  28. Harada, M.L., H. Schneider, M.P.C. Schneider, I. Sampaio, J. Czelusniak &; M. Goodman, 1995. DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. Mol. Biol. Evol. 4(3): 331-349.Google Scholar
  29. Hasegawa, M.H., H. Kishino &; T. Yano, 1989. Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in Hominidae. J. Hum. Evol. 18: 461-476.Google Scholar
  30. Hoelzer, G.A., J. Wallman &; D.J. Melnick, 1998. The effects of social structure, geographical structure, and population size on the evolution of mitochondrial DNA. II. Molecular clocks and the lineage sorting period. J. Mol. Evol. 47: 21-31.Google Scholar
  31. Horovitz, I., 1999. A phylogenetic study of living and fossil platyrrhines. Amer. Museum Novitates 3269, 1-40.Google Scholar
  32. Horovitz, I., R. Zardoya &; A. Meyer, 1998. Platyrrhine systematics: a simultaneous analysis of molecular and morphological data. Am. J. Phys. Anthropol. 106: 261-281.Google Scholar
  33. Irwin, D.M., T.D. Kocher &; A.C. Wilson, 1991. Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128-144.Google Scholar
  34. Jukes, T.H. &; C.R. Cantor, 1969. Evolution of protein molecules, pp. 21-132 in Mammalian Protein Metabolism, edited by H.N. Munro. Academic Press, N.Y.Google Scholar
  35. Kappeler, P.M., 1997. Determinants of primate social organization: comparative evidence and new insights from Malagasy Lemurs. Biol. Rev. 72: 111-151.Google Scholar
  36. Kimura, M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120.Google Scholar
  37. Kinzey, W.G., 1979. Distribution of primates and forest refuges, pp. 8-13 in Biological Diversification in the Tropics, Proc. 5th Intern. Symp. Assoc. Tropical Biology.Google Scholar
  38. Kumar, S., K. Tamura &; M. Nei, 1993. MEGA-Molecular Evolutionary Genetics Analysis (version 1.0). Computer program distributed by the Pennsylvania State University, University Park, PA 16802.Google Scholar
  39. Kumar, S., K. Tamura, I.B. Jakobsen &; M. Nei, 2001. MEGA2:Molecular Evolutionary Genetics Analysis software. Bioinformatics (submitted).Google Scholar
  40. Li, W.-H., M. Tanimura &; P.M. Sharp, 1987. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J. Mol. Evol. 25: 330-342.Google Scholar
  41. Li, W.-H., M. Gouy, P. Sharp, C. O'Huigin &; Y.-W. Yang, 1990. Molecular phylogeny of Rodentia, Lagomorpha, Artiodactyla and Carnivora and molecular clocks. Proc. Natl. Acad. Sci. USA 87: 6703-6707.Google Scholar
  42. Martin, A.P., 1995. Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol. Biol. Evol. 12: 1124-1131.Google Scholar
  43. Martin, A.P., G. Naylor &; S.R. Palumbi, 1992. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357: 153-155.Google Scholar
  44. Martin, A.P. &; S.R. Palumbi, 1993. Body size, metabolic rate, generation time and the molecular clock. Proc. Natl. Acad. Sci. USA 90: 4087-4091.Google Scholar
  45. Medeiros, M.A., R.M.S. Barros, J.C. Pieczarka, C.Y. Nagamochi, M. Pansa, M. Garcia, F. Garcia &; J. Egozcue, 1997. Radiation and Speciation of spider monkeys genus Ateles, from the cytogenetic viewpoint. Am. J. Primatol. 42: 167-178.Google Scholar
  46. Mendoza, S.P., E.L. Lowe &; S. Levine, 1978. Social organization and social behavior in two subspecies of squirrel monkeys (Saimiri sciureus). Folia Primatol. (Basel) 30 (2): 126-144.Google Scholar
  47. Meireles, C.M., M.P.C. Schneider, M.I.C. Sampaio, H. Schneider, J.L. Slightom, C.H. Chiu, K. Neiswanger, D.L. Gumucio, J. Czelusniak &; M. Goodman, 1995. Fate of a redundant γ-globin gene in the atelid clade of New World monkeys: implications concerning fetal globin gene expression. Proc. Natl. Acad. Sci. USA 92: 2607-2611.Google Scholar
  48. Meireles, C.M., J. Czelusniak, M.P.C. Schneider, J.A.P.C. Muniz, M.C. Brigido, H.S. Ferreira &; M. Goodman, 1999. Molecular phylogeny of ateline NewWorld monkeys (Platyrrhini, Atelinae) based on γ-globin gene sequences: evidence that Brachyteles is the sister group of Lagothrix. Mol. Phylogenet. Evol. 12(1): 10-30.Google Scholar
  49. Milton, K., 1982. Dietary quality and demographic regulation in a howler monkey population, pp. 273-290 in The Ecology of a Tropical Forest Seasonal Rhythms and Long Term Changes, edited by E.G. Leigh, Jr., A.S. Rand &; D.M. Windsor. Smithsonian Institution Press, Washington D.C.Google Scholar
  50. Mooers, A. &; P.H. Harvey, 1994. Metabolic rate, generation time and the rate of molecular evolution in birds. Mol. Phylogenet. Evol. 3: 344-350.Google Scholar
  51. Morton, B.R., 1993. Chloroplast DNA codon use: evidence for selection at the psb a locus based on tRNA availability. J. Mol. Evol. 37: 273-280.Google Scholar
  52. Ohta, T., 1996. The current significance and standing of neutral theories. Bioessays 18(8): 673-677.Google Scholar
  53. Ohta, T., 1993. An examination of the generation time effect on molecular evolution. Proc. Natl. Acad. Sci. USA 90: 10676-10680.Google Scholar
  54. Patton, J.L. &; M.F. Smith, 1992. mtDNA phylogeny of Andean mice: a test of diversification across ecological gradients. Evolution 46: 174-183.Google Scholar
  55. Patton, J.L, M.N.F. da Silva &; J.R. Malcom, 1994. Gene genealogy and differentation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon Basin: a test of the riverine barrier hypothesis. Evolution 48: 1314-1323.Google Scholar
  56. Peres, C.A., J.L. Patton &; M.N.F. da Silva, 1996. Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatol. 67: 113-124.Google Scholar
  57. Piaggio, A.J. &; G.S. Spicer, 2001. Molecular phylogeny of the chipmunks inferred from Mitochondrial cytochrome b and cytochrome oxidase II gene sequences. Mol. Phylogenet. Evol. 20(3): 335-350.Google Scholar
  58. Robinson, J.G. &; C.H. Janson, 1986. Capuchins, Squirrel Monkeys, and Atelines: socioecological convergence with Old World Primates, pp. 69-82 in Primate Societies, edited by B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham &; T.T. Struhsaker. Chicago Press University, Chicago.Google Scholar
  59. Rosenberger, A.L. &; K.B. Strier, 1989. Adaptive radiation of the ateline primates. J. Hum. Evol. 18: 717-750.Google Scholar
  60. Ruvolo, M., T.R. Disotell, M.W. Allard, W.M. Brown &; R.L. Honeycutt, 1991. Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc. Natl. Acad. Sci. USA 88: 1570-1574.Google Scholar
  61. Ruvolo, M., S. Zehr, M. von Dormun, D. Pan, B. Chang &; J. Lin, 1993. Mitochondrial COII sequences and modern human origins. Mol. Biol. Evol. 10(6): 1115-1135.Google Scholar
  62. Rylands, A.B., H. Schneider, A. Langguth, R.A. Mittermeier, C.P. Groves &; E. Rodríguez-Luna, 2000. An assessment of the diversity of NewWorld Primates. Neotrop. Primates 8(2): 61-93.Google Scholar
  63. Saitou, N. &; M. Nei, 1987. The Neighbor-Joining Method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.Google Scholar
  64. Seino, S., G.I. Bell &; W.-H. Li, 1992. Sequences of primate insulin genes support the hypothesis of a slower rate of molecular evolution in humans and apes than in monkeys. Mol. Biol. Evol. 9: 193-203.Google Scholar
  65. Sharp, P.M., T.M.F. Tuohy &; K.R. Mosurski, 1986. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucl. Acids Res. 14: 5125-5143.Google Scholar
  66. Shields, D.C., P.M. Sharp, D.G. Higgins &; F. Wright, 1988. 'silent’ sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol. Biol. Evol. 5: 704-716.Google Scholar
  67. Schneider, H., M.P.C. Schneider, I. Sampaio, M.L. Harada, M. Stanhope, J. Czelusniak &; M. Goodman, 1993. Molecular phylogeny of the New World Monkeys (Platyrrhini, Primates). Mol. Phylogenet. Evol. 2: 225-242.Google Scholar
  68. Schneider, H., I. Sampaio, M.L. Harada, C.M.L. Barroso, M.P.C. Schneider, J. Czelusniak &; M. Goodman, 1996. Molecular phylogeny of the New World Monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron1 and γ-globin sequences. Am. J. Phys. Anthropol. 100: 153-179.Google Scholar
  69. Strier, K.B., 1996. Reproductive ecology of female muriquis, pp. 511-532 in Adaptative Radiations of Neotropical Primates, edited by M. Norconk, A. Rosenberger &; P. Garber. Plenum Press, N.Y.Google Scholar
  70. Tagliaro, C.H., M.P.C. Schneider, H. Schneider, I.C. Sampaio &; M.J. Stanhope, 1997. Marmoset phylogenetics, conservation perspectives, and evolution of mtDNA control region. Mol. Biol. Evol. 14: 674-684.Google Scholar
  71. Tajima, F., 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135: 599-607.Google Scholar
  72. Tkezaki, N., A. Rzhetsky &; M. Nei, 1995. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12: 823-833.Google Scholar
  73. Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin &; D.G. Higgins, 1997. The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24: 4876-4882.Google Scholar
  74. Yoder, A.D., R. Vilgalys &; M. Ruvolo, 1996. Molecular evolutionary dynamics of cytochrome b in strepsirrhine primates: the phylogenetic significance of third-position transversions. Mol. Biol. Evol. 13(10): 1339-1350.Google Scholar
  75. von Dornum, M. &; M. Ruvolo, 1999. Phylogenetic relationships of the New World monkeys (Primates, Platyrrhini) based on nuclear G6PD DNA sequences. Mol. Phylogenet. Evol. 11(3): 459-476.Google Scholar
  76. Walsh, P.S., D.A. Metzger &; R. Higuchi, 1991. ChelexΠ100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Bio Tech. 10(4): 506-513.Google Scholar
  77. Wright, F., 1990. The ‘effective number of codons’ used in a gene. Gene 87: 23-29.Google Scholar
  78. Wu, C.-I. &; W.-H Li, 1985. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc. Natl. Acad. Sci. USA 82: 1741-1745.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Marina S. Ascunce
    • 1
  • Esteban Hasson
    • 1
  • Marta D. Mudry
    • 1
  1. 1.GIBE (Grupo de Investigación en Biología Evolutiva), Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales (FCEN)Universidad de Buenos Aires (UBA), Ciudad UniversitariaBuenos AiresArgentina (Phone

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