Skip to main content
Log in

Patterns of C-heterochromatin and telomeric DNA in two representative groups of small apes, the genera Hylobates and Symphalangus

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The course of chromosome evolution in small apes is still not clear, though painting analyses have opened the way for elucidating the puzzle. Even the C-banding pattern of the lar-group of gibbons (the genus Hylobates) is not clarified yet, although our previous studies suggested that lar-group gibbons have a unique C-banding pattern. We therefore made observations to establish C-banded karyotypes of the agile gibbons included in the lar-group. The data were compared with those of siamangs (the genus Symphalangus), which carry distinctive C-bands, to determine the chromosomal patterns in each group. C-banded chromosomes of agile gibbons showed several terminal, interstitial and paracentric bands, whose patterns are specific for each chromosome, whereas the C-bands of siamangs were located only at the terminal and centromeric regions in most chromosomes. Moreover, the C-bands of agile gibbons and siamangs were shown to be G+C-rich and A+T-rich DNA, respectively, by DAPI/C-band sequential staining. Additionally, PRINS labelling with a telomere primer revealed that agile gibbons have telomeric DNA only at chromosome ends where there is no C-band (non-telomeric heterochromatin), whereas the telomeric DNA of siamangs is located in the terminal C-banded regions (telomeric heterochromatin). Although the evolutionary mechanisms in small apes are still unknown, C-banding patterns and distribution of telomeric DNA sequences should provide valuable data to deduce the evolutionary pathways of small apes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alberts B, Johnson A, Lewis J et al. (2002) Molecular Biology of The Cell, 4th edn. New York: Garland Science.

    Google Scholar 

  • Arnold N, Stanyon R, Jauch A, O'Brien P, Wienberg J (1996) Identification of complex chromosome rearrangements in the gibbon by fluorescent in situ hybridization (FISH) of a human chromosome 2q specific microlibrary, yeast artificial chromosomes, and reciprocal chromosome painting. Cytogenet Cell Genet 74: 80–85.

    PubMed  Google Scholar 

  • Brandon-Jones D, Eudey AA, Geissmann T et al. (2004) Asian primate classification. Int J Primatol 25: 97–164.

    Article  Google Scholar 

  • Garza JC, Woodruff DS (1992) A phylogenetic study of the gibbons (Hylobates) using DNA obtained noninvasively from hair. Mol Phylogenet Evol 1: 202–210.

    Article  PubMed  Google Scholar 

  • Groves CP (1984) A new look at the taxonomy and phylogeny of the gibbons. In: Preuschoft H, Chives DJ, Brockelman W, Creel N, eds. The Lesser Apes. Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Groves CP (1989) A Theory of Human and Primate Evolution. Oxford: Clarendon Press.

    Google Scholar 

  • Guillén AKZ, Hirai Y, Tanoue T, Hirai H (2004) Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Res 12: 225–237.

    Article  PubMed  Google Scholar 

  • Hall LM, Jones DS, Wood BA (1998) Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. Mol Phylogenet Evol 10: 281–286.

    Article  PubMed  Google Scholar 

  • Hayashi S, Hayasaka K, Takenaka O, Horai S (1995) Molecular phylogeny of gibbons inferred from mitochondrial DNA sequences: preliminary report. J Mol Evol 41: 359–365.

    Article  PubMed  Google Scholar 

  • Hirai H (2001) Relationship of telomere sequence and constitutive heterochromatin in the human and apes as detected by PRINS. Meth Cell Sci 23: 29–35.

    Article  Google Scholar 

  • Hirai H, Taguchi T, Godwin AK (1999) Genomic differentiation of 18 S ribosomal DNA and β-satellite DNA in the hominoid and its evolutionary aspects. Chromosome Res 7: 531–540.

    Article  PubMed  Google Scholar 

  • Hirai H, Hirai Y, Kawamoto Y et al. (2002) Cytogenetic differentiation of two sympatric tree shrew taxa found in the southern part of the Isthmus of Kra. Chromosome Res 10: 313–327.

    Article  PubMed  Google Scholar 

  • Hirai H, Mootnick AR, Takenaka O et al. (2003) Genetic mechanism and property of a whole-arm translocation (WAT) between chromosomes 8 and 9 of agile gibbons (Hylobates agilis). Chromosome Res 11: 37–50.

    Article  PubMed  Google Scholar 

  • Hirai H, Matsubayashi K, Kumazaki K et al. (2005) Chimpanzee chromosome: retrotransposable compound repeat DNA organization (RCRO) and its influence on meiotic prophase and crossing-over. Cytogenet Genome Res 108: 248–254.

    Article  PubMed  Google Scholar 

  • Imai HT (1991) Mutability of constitutive heterochromatin (C-bands) during eukaryotic chromosome evolution and their cytological meaning. Jpn J Genet 66: 635–661.

    PubMed  Google Scholar 

  • Jauch A, Wienberg J, Stanyon R et al. (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci USA 89: 8611–8615.

    PubMed  Google Scholar 

  • Koehler U, Arnold N, Weinberg J, Tofanelli S, Stanyon R (1995) Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization. Am J Phys Anthropol 97: 37–47.

    PubMed  Google Scholar 

  • Liu R, Shi L, Chen Y (1987) A study on the chromosomes of white-browed gibbon (Hylobates hoolock leuconedys). Acta Theriologia Sinica 7: 1–7 (in Chinese with English abstract).

    Google Scholar 

  • Marks J (1993) Hominoid heterochromatin: Terminal C-bands as a complex genetic trait linking chimpanzee and gorilla. Am J Phys Anthropol 90: 237–246.

    Article  PubMed  Google Scholar 

  • Müller S, Hollatz M, Wienberg J (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113: 493–501.

    Article  PubMed  Google Scholar 

  • Multani AS, Ozen M, Furlong CL et al. (2001) Heterochromatin and interstitial telomeric DNA homology. Chromosoma 110: 214–220.

    PubMed  Google Scholar 

  • Myers RH, Shaver DA (1979) Hybrid ape offspring of mating of gibbon and siamang. Science 205: 308–310.

    PubMed  Google Scholar 

  • Nie W, Rens W, Wang J, Yang F (2001) Conserved chromosome segment in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92: 248–253.

    Article  PubMed  Google Scholar 

  • Pellicciari C, Formenti D, Zuccotti M et al. (1988) Genome size and constitutive heterochromatin in Hylobates muelleri and Symphalangus syndactylus and in their viable hybrid. Cytogenet Cell Genet 47: 1–4.

    PubMed  Google Scholar 

  • Ross C, Giessmann T (2001) Molecular phylogeny of the major hylobatid divisions. Mol Phylogenet Evol 19: 486–494.

    Article  PubMed  Google Scholar 

  • Stanyon R, Chiarelli B, Gottlieb K, Patton WH (1986) The phylogenetic and taxonomic status of Pan paniscus: A chromosomal perspective. Am J Phys Anthropol 69: 489–498.

    Article  Google Scholar 

  • Stanyon R, Sineo L, Chiarelli B et al. (1987) Banded karyotype of the 44-chromosome gibbons. Folia Primatol 48: 56–64.

    Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromere heterochromatin. Exp Cell Res 75: 304–306.

    Article  PubMed  Google Scholar 

  • Sumner AT (1990) Chromosome Banding. London: Unwin Hyman.

    Google Scholar 

  • Sumner AT (2003) Chromosomes: Organization and Function. Oxford: Blackwell Scientific.

    Google Scholar 

  • van Tuinen P, Ledbetter DH (1983) Cytogenetic comparison and phylogeny of three species of Hylobatidae. Am J Phys Anthropol 61: 453–466.

    PubMed  Google Scholar 

  • van Tuinen P, Mootnick AR, Kingswood SC, Hale DW, Kumamoto AT (1999) Complex, compound inversion/translocation polymorphism in an ape: Presumptive intermediate stage in the karyotypic evolution of the agile gibbon Hylobates agilis. Am J Phys Antrophol 110: 129–142.

    Article  Google Scholar 

  • Viegas-Péquignot E, Derbin C, Malfoy B et al. (1983) Z-DNA immunoreactivity in fixed metaphase chromosomes of primates. Proc Natl Acad Sci USA 80: 5890–5894.

    PubMed  Google Scholar 

  • Wienberg J, Stanyon R (1987) Fluorescent heterochromatin staining in primate chromosomes. Hum Evol 2: 445–457.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hirohisa Hirai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wijayanto, H., Hirai, Y., Kamanaka, Y. et al. Patterns of C-heterochromatin and telomeric DNA in two representative groups of small apes, the genera Hylobates and Symphalangus. Chromosome Res 13, 715–722 (2005). https://doi.org/10.1007/s10577-005-1007-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-005-1007-4

Key words

Navigation