The Gibbons pp 37-49 | Cite as

Genetic Differentiation of Agile Gibbons Between Sumatra and Kalimantan in Indonesia

  • Hirohisa Hirai
  • Azusa Hayano
  • Hiroyuki Tanaka
  • Alan R. Mootnick
  • Hery Wijayanto
  • Dyah Perwitasari-Farajallah
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


The gibbons (Hylobatidae) are a diverse group of small apes that have adapted to the rain forests of South and Southeast Asia and radiated into numerous (12–14) discrete species. Recently, the four subgenera of small apes [Hoolock, (previously Bunopithecus, Mootnick and Groves 2005), Hylobates, Symphalangus, and Nomascus] were all raised to the level of genera because the genetic distances between them indicated by mitochondrial DNA were larger than those between Homo and Pan (Hayashi et al. 1995; Roos and Geissmann 2001). Some aspects of gibbon classification are still controversial, in particular the differentiation of subspecies (Groves 2001; Brandon-Jones et al. 2004; Mootnick 2006; Chatterjee this volume). Accurate determination of collection localities is critical for diagnosing subspecies in this group, which is morphologically very diverse in some physical features (e.g., pelage pattern, Marshall and Sugardjito 1986; Mootnick 2006). Thus it is important to use...


Chromosome Evolution Chromosome Change Zoological Institution Captive Parent Agile Gibbon 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was permitted and helped by the Indonesian Research Authority (LIPI) and by Indonesian institutions (PHKA, BKSDA, PSSP-IPB, Safari Park, Ragunan Zoo, Bukit Tinggi Zoo, National Resource Conservation Offices, Animal Quarantine Department etc.), and supported by The Japan Society for Promotion of Science Grants (Oversea Research 1440520 to H.H.) and by a Grant for the Biodiversity Research of the 21st Century COE (A14) and the Global COE (A06).


  1. Brandon-Jones, D., Eudey, A.A., Geissmann, T., Groves, C.P., Melnick, D.J., Morales, J.C., Shekelle, M. and Stewart, C.B. 2004. Asian primate classification. International Journal of Primatology 25:97–163.CrossRefGoogle Scholar
  2. Clement, M., Posada, D. and Crandall, K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9:1657–1659.PubMedCrossRefGoogle Scholar
  3. Crandall, K.A., Bininda-Emonds, O.R.P., Mace, G.M. and Wayne, R.K. 2000. Considering evolutionary processes in conservation biology: an alternative to 'evolutionarily significant units'. Trends in Ecology and Evolution 15:290–295.PubMedCrossRefGoogle Scholar
  4. Cronin, J.E., Sarich, V.M. and Ryder, O. 1984. Molecular evolution and speciation in the lesser apes. In The Lesser Apes, H. Preuschoft, D.J. Chivers, W.Y. Brockelman and N. Creel (eds.), pp. 467–485. Edinburgh: Edinburgh University Press.Google Scholar
  5. Excoffier, L., Smouse, P.T. and Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distance among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491.PubMedGoogle Scholar
  6. Frankham, R., Ballou, J.D. and Briscoe, D.A. 2002. Introduction to Conservation Genetics. Cambridge: Cambridge University Press.Google Scholar
  7. Geissmann, T. 1995. Gibbon systematics and species identification. International Zoo News 42:467–501.Google Scholar
  8. Groves, C.P. 1972. Systematics and phylogeny of gibbons. In Gibbon and Siamang. Vol. 1: Evolution, Ecology, Behavior, and Captive Maintenance, D.M. Rumbaugh (ed.), pp. 1–89. Basel: Karger.Google Scholar
  9. Groves, C.P. 2001. Primate Taxonomy. Washington: Smithsonian Institution Press.Google Scholar
  10. Hayashi, S., Hayasaka, K., Takenaka, O. and Horai, S. 1995. Molecular phylogeny of gibbons inferred from mitochondrial DNA sequence: preliminary report. Journal of Molecular Evolution 41:359–365.PubMedCrossRefGoogle Scholar
  11. Hirai, H. 2004. A report of the Japan Society for Promotion of Science Grants (Oversea Research 1440520): Comprehensive study of subspeciation of agile gibbons. (Japanese with some English chapters.).Google Scholar
  12. Hirai, H., Wijayanto, H., Tanaka, H., Mootnick, A.R., Hayano, A., Perwitasari-Farajallah, D., Iskandriati, D. and Sajuthi, D. 2005. A whole-arm translocation (WAT8/9) separating Sumatran and Bornean agile gibbons, and its evolutionary features. Chromosome Research 13:123–133.PubMedCrossRefGoogle Scholar
  13. Hirai, H., Mootnick, A.R., Takenaka, O., Suryobroto, B., Mouri, T., Kamanaka, Y., Katoh, A., Kimura, N., Katoh, A. and Maeda, N. 2003. Genetic mechanism and property of a whole-arm translocation (WAT) between chromosomes 8 and 9 of agile gibbons (Hylobates agilis). Chromosome Research 11:37–50.PubMedCrossRefGoogle Scholar
  14. Imai, H.T. 1983. Quantitative analysis of karyotype alteration and species differentiation in mammals. Evolution 37:1154–1161.Google Scholar
  15. Jauch, A., Wienberg, J., Stanyon, R., Arnold, N., Tofanelli, S., Ishida, T. and Cremer, T. 1992. Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proceedings of the National Academy of Sciences 89:8611–8615.CrossRefGoogle Scholar
  16. Kim, H., Hirai, H. and Takenaka, O. 1996. Molecular features of the TSPY gene of gibbons and old world monkeys. Chromosome Research 4:500–506.PubMedCrossRefGoogle Scholar
  17. Koehler, U., Bigoni, F., Wienberg, J. and Stanyon, R. 1995. Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287–292.PubMedCrossRefGoogle Scholar
  18. Marshall, J. and Sugardjito, J. 1986. Gibbon systematics. In Comparative Primate Biology, Vol. 1: Systematics, Evolution, and Anatomy, D.R. Swindler and J. Erwin (eds.), pp. 137–185. New York: Alan R. Liss.Google Scholar
  19. Mootnick, A.R. 2006. Gibbon (Hylobatidae) species identification recommended for rescue or breeding centers. Primate Conservation 21:103–138.CrossRefGoogle Scholar
  20. Mootnick, A.R. and Groves, C.P. 2005. A new generic name for the Hoolock gibbon (Hylobatidae). International Journal of Primatology 26:971–976.CrossRefGoogle Scholar
  21. Müller, S., Hollatz, M. and Weinberg, J. 2003. Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Human Genetics 113:493–501.PubMedCrossRefGoogle Scholar
  22. Nie, W., Rens, W., Wang, J. and Yang, F. 2001. Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenetics and Cell Genetics 92:248–253.PubMedCrossRefGoogle Scholar
  23. Roos, C.I. and Geissmann, T. 2001. Molecular phylogeny of the major hylobatid divisions. Molecular Phylogenetics and Evolution 19:486–494.PubMedCrossRefGoogle Scholar
  24. Schneider, S., Roessli, D. and Excoffier, L. 2000. Arlequin ver. 2.000: A software for population genetics data analysis. Genetics and Biochemistry Laboratory, University of Geneva, Switzerland.Google Scholar
  25. Stanyon, R., Sineo, L., Chiarelli, B., Camperio-Ciani, A., Haimoff, A.R., Mootnick, A.R. and Sutarman, D. 1987. Banded karyotypes of the 44-chromosome gibbons. Folia Primatologica 48:56–64.CrossRefGoogle Scholar
  26. Swofford, D.L. 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sunderland, MA: Sinauer Associates.Google Scholar
  27. Tanaka, H., Wijayanto, H., Mootnick, A.R., Iskandriati, D., Perwitasari-Farajallah, D., Sajuthi, D. and Hirai, H. 2004. Molecular phylogenetic analyses of subspecific relationships in agile gibbons (Hylobates agilis) using mitochondrial and TSPY gene sequences. Folia Primatologica 75(suppl 1):418.Google Scholar
  28. Tantravahi, R., Dev, V.G., Frischein, L.L., Miller, O.A. and Miller, O.J. 1975. Karyotype of the gibbons Hylobates lar and H. moloch. Cytogenetics and Cell Genetics 15:92–102.PubMedCrossRefGoogle Scholar
  29. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. 1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tolls. Nucleic Acids Research 25:4876–4882.PubMedCrossRefGoogle Scholar
  30. van Tuinen, P. and Ledbetter, D.H. 1983. Cytogenetic comparison and phylogeny of three species of Hylobatidae. American Journal of Physical Anthropology 61:453–466.PubMedCrossRefGoogle Scholar
  31. van Tuinen, P., Mootnick, A.R., Kingswood, S.C., Hale, D.W. and Kunamoto, A.T. 1999. Complex, compound inversion/translocation polymorphism in an ape: presumptive intermediates stage in the karyotypic evolution of the agile gibbon Hylobates agilis. American Journal of Physical Anthropology 110:129–142.PubMedCrossRefGoogle Scholar
  32. White, M.J. 1978. Modes of Speciation. San Francisco: W. H. Freeman and Company.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Hirohisa Hirai
    • 1
  • Azusa Hayano
    • 1
  • Hiroyuki Tanaka
    • 1
  • Alan R. Mootnick
    • 2
  • Hery Wijayanto
    • 3
    • 4
  • Dyah Perwitasari-Farajallah
    • 3
    • 4
  1. 1.Primate Research Institute, Kyoto UniversityInuyamaJapan
  2. 2.Gibbon Conservation CenterSanta ClaritaUSA
  3. 3.Primate Research Center, Bogor Agricultural UniversityBogor 16151
  4. 4.Department of Veterinary AnatomyGadjah Mada UniversityYogyakarta1Indonesia

Personalised recommendations