Human Genetics

, Volume 113, Issue 6, pp 493–501 | Cite as

Chromosomal phylogeny and evolution of gibbons (Hylobatidae)

  • Stefan Müller
  • Melanie Hollatz
  • Johannes Wienberg
Original Investigation

Abstract

Although human and gibbons are classified in the same primate superfamily (Hominoidae), their karyotypes differ by extensive chromosome reshuffling. To date, there is still limited understanding of the events that shaped extant gibbon karyotypes. Further, the phylogeny and evolution of the twelve or more extant gibbon species (lesser apes, Hylobatidae) is poorly understood, and conflicting phylogenies have been published. We present a comprehensive analysis of gibbon chromosome rearrangements and a phylogenetic reconstruction of the four recognized subgenera based on molecular cytogenetics data. We have used two different approaches to interpret our data: (1) a cladistic reconstruction based on the identification of ancestral versus derived chromosome forms observed in extant gibbon species; (2) an approach in which adjacent homologous segments that have been changed by translocations and intra-chromosomal rearrangements are treated as discrete characters in a parsimony analysis (PAUP). The orangutan serves as an "outgroup", since it has a karyotype that is supposed to be most similar to the ancestral form of all humans and apes. Both approaches place the subgenus Bunopithecus as the most basal group of the Hylobatidae, followed by Hylobates, with Symphalangus and Nomascus as the last to diverge. Since most chromosome rearrangements observed in gibbons are either ancestral to all four subgenera or specific for individual species and only a few common derived rearrangements at subsequent branching points have been recorded, all extant gibbons may have diverged within relatively short evolutionary time. In general, chromosomal rearrangements produce changes that should be considered as unique landmarks at the divergence nodes. Thus, molecular cytogenetics could be an important tool to elucidate phylogenies in other species in which speciation may have occurred over very short evolutionary time with not enough genetic (DNA sequence) and other biological divergence to be picked up.

Supplementary material

Supplementary 1 Summary of all observed adjacent CSHs in the karyotypes of the four gibbon species and the orangutan

supp1.pdf (15 kb)
(PDF 16 KB)

Supplementary 2 Presence (“1) or absence (“0”) of each observed adjacent CSHs in the karyotypes of the four gibbon species and the orangutan (Pongo pygmaeus, PPY; B. hoolock, BHO; H. lar, HLA; S. syndactylus, SSY; N. concolor, NCO)

supp2.pdf (27 kb)
(PDF 28 KB)

References

  1. 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 74:80–85PubMedGoogle Scholar
  2. Bender MA, Chu EHY (1963) The chromosomes of primates. In: Buettner-Janusch J (ed) Evolutionary and genetic biology of primates, vol 1. Academic Press, New York, pp 261–310Google Scholar
  3. Bruce EJ, Ayala FJ (1979) Phylogenetic relationships between man and the apes: electrophoretic evidence. Evolution 33:1040–1056Google Scholar
  4. Couturier J, Lernould J-M (1991) Karyotypic study of four gibbon forms provisionally considered as subspecies of Hylobates (Nomascus) concolor (Primates, Hylobatidae). Folia Primatol (Basel) 56:95–104Google Scholar
  5. Couturier J, Dutrillaux B, Turleau C, Grouchy J de (1982) Comparative karyotyping of our gibbon species or subspecies. Ann Génét (Paris) 25:5–10Google Scholar
  6. Créau-Goldberg N (1993) Primate genetic maps. In: O´Brien SJ (ed) Genetic maps, locus maps of complex genomes; nonhuman vertebrates, vol 4. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  7. Dutrillaux B, Rethore MO, Aurias A, Goustard M (1975) Karyotype analysis of 2 species of gibbons (Hylobates lar and H. concolor) with different banding species. Cytogenet Cell Genet 15:81–91PubMedGoogle Scholar
  8. Garza JC, Woodruff DS (1992) A phylogenetic study of the gibbons (Hylobates) using DNA obtained noninvasively from hair. Mol Phylogenet Evol 1:202–210PubMedGoogle Scholar
  9. Geissmann T (2002) Taxonomy and evolution of gibbons. In: Soligo C, Anzenberger G, Martin RD (eds).Anthropology and primatology into the third millennium: the centenary congress of the Zürich Anthropological Institute. Evolutionary anthropology, vol 11, supplement 1. Wiley-Liss, New York, pp 28–31Google Scholar
  10. Groves CP (1972) Systematics and phylogeny of gibbons. In: Rumbaugh DM (ed) Gibbon and siamang, vol 1. Karger, Basel, pp 1–89Google Scholar
  11. Haimoff EH, Chivers DJ, Gittins SP, Whitten T (1982) A phylogeny of gibbons (Hylobates spp) based on morphological and behavioural characters. Folia Primatol (Basel) 39: 213–237Google Scholar
  12. Hall LM, Jones D, Wood B (1996) Evolutionary relationships between gibbon subgenera inferred from DNA sequence data. Biochem Soc Trans 24:416SPubMedGoogle Scholar
  13. Hall LM, Jones DS, Wood BA (1998) Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. Mol Phylogenet Evol 10:281–286CrossRefPubMedGoogle Scholar
  14. Jauch A, Wienberg J, Stanyon R, Arnold N, Tofanelli S, Ishida T, Cremer T (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci USA 89:8611–8615PubMedGoogle Scholar
  15. Koehler U, Arnold N, Wienberg J, Tofanelli S, Stanyon R (1995a) Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization. Am J Phys Anthropol 97:37–47PubMedGoogle Scholar
  16. Koehler U, Bigoni F, Wienberg J, Stanyon R (1995b) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287–292CrossRefPubMedGoogle Scholar
  17. Marks J (1982) Evolutionary tempo and phylogenetic inference based on primate karyotypes. Cytogenet Cell Genet 34:261–264PubMedGoogle Scholar
  18. Müller S, Wienberg J (2001) "Bar-coding" primate chromosomes: molecular cytogenetic screening for the ancestral hominoid karyotype. Hum Genet 109:85–94PubMedGoogle Scholar
  19. Müller S, O'Brien PC, Ferguson-Smith MA, Wienberg J (1998) Cross-species colour segmenting: a novel tool in human karyotype analysis. Cytometry 33:445–452CrossRefPubMedGoogle Scholar
  20. Müller S, Neusser M, Wienberg J (2002) Towards unlimited colors for fluorescence in-situ hybridization (FISH). Chromosome Res 10:223–232CrossRefPubMedGoogle Scholar
  21. Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, LondonGoogle Scholar
  22. Nie W, Rens W, Wang J, Yang F (2001) Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92:248–253CrossRefPubMedGoogle Scholar
  23. Prouty LA, Buchanan PD, Pollitzer WS, Mootnick AR (1983) A presumptive new hylobatid subgenus with 38 chromosomes. Cytogenet Cell Genet 35:141–142PubMedGoogle Scholar
  24. Rokas A, Holland WH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459Google Scholar
  25. Roos C, Geissmann T (2001) Molecular phylogeny of the major hylobatid divisions. Mol Phylogenet Evol 19:486–494CrossRefPubMedGoogle Scholar
  26. Schröck E, du Manoir S, Veldman T, Schoell B, Wienberg J, Ferguson-Smith MA, Ning Y, Ledbetter DH, Bar-Am I, Soenksen D, Garini Y, Ried T (1996) Multicolor spectral karyotyping of human chromosomes. Science 273:494–497PubMedGoogle Scholar
  27. Speicher MR, Gwyn Ballard S, Ward DC (1996) Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nat Genet 12:368–375PubMedGoogle Scholar
  28. Stanyon R, Chiarelli B (1983) Mode and tempo in primate chromosomal evolution: implications for hylobatid phylogeny. J Hum Evol 10:305–315Google Scholar
  29. Stanyon R, Sineo L, Chiarelli B, Camperio-Ciani A, Haimoff EH, Mootnick AR, Suturman DR (1987) Banded karyotypes of the 44-chromosome gibbons. Folia Primatol (Basel) 48:56–64Google Scholar
  30. Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4th edn. Sinauer Associates, Sunderland, Mass.Google Scholar
  31. Telenius H, Pelmear AHP, Tunnacliffe A, Carter NP, Behmel A, Ferguson-Smith MA, Nordenskjold M, Pfragner R, Ponder BAJ (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosome Cancer 4:257–263Google Scholar
  32. Turleau C, Creau-Goldberg N, Cochet C, Grouchy J de (1983) Gene mapping of the gibbon. Its position in primate evolution. Hum Genet 64:65–72PubMedGoogle Scholar
  33. Van Tuinen P, Ledbetter DH (1983) Cytogenetic comparison and phylogeny of three species of Hylobatidae. Am J Phys Anthropol 61:453–466PubMedGoogle Scholar
  34. Van Tuinen P, Ledbetter DH (1989) New confirmatory and regional gene assignments in the white-cheeked gibbon Hylobates concolor. Cytogenet Cell Genet 51:1094–1095Google Scholar
  35. 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 Anthropol 110:129–142CrossRefPubMedGoogle Scholar
  36. Wienberg J, Jauch A, Stanyon R, Cremer T (1990) Molecular cytotaxonomy of primates by chromosomal in situ suppression hybridization. Genomics 8:347–350PubMedGoogle Scholar
  37. Wienberg J, Stanyon R, Jauch A, Cremer T (1992) Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma 101:265–270PubMedGoogle Scholar
  38. Wienberg J, Frönicke L, Stanyon R (2000) Insights into mammalian genome organization and evolution by molecular cytogenetics. In: Clark MS (ed) Comparative genomics. Kluver, Dordrecht, pp 207–244Google Scholar
  39. Wurster DH, Benirschke K (1969) Chromosomes of some primates. Mamm Chromosome Newsletter 10:3Google Scholar
  40. Yu D, Yang F, Liu R (1997) A comparative chromosome map between human and Hylobates hoolock built by chromosome painting. Yi Chuan Xue Bao 24:417–423PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Stefan Müller
    • 1
  • Melanie Hollatz
    • 1
  • Johannes Wienberg
    • 1
    • 2
  1. 1.Institut für Anthropologie und Humangenetik, Department Biologie IILudwig-Maximilians-UniversitätMunichGermany
  2. 2.Institute of Human GeneticsGSF—National Research Center for Environment and HealthMunichGermany

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