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.
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References
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
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 261–310
Bruce EJ, Ayala FJ (1979) Phylogenetic relationships between man and the apes: electrophoretic evidence. Evolution 33:1040–1056
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) 56:95–104
Couturier J, Dutrillaux B, Turleau C, Grouchy J de (1982) Comparative karyotyping of our gibbon species or subspecies. Ann Génét (Paris) 25:5–10
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, NY
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 15:81–91
Garza JC, Woodruff DS (1992) A phylogenetic study of the gibbons (Hylobates) using DNA obtained noninvasively from hair. Mol Phylogenet Evol 1:202–210
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 28–31
Groves CP (1972) Systematics and phylogeny of gibbons. In: Rumbaugh DM (ed) Gibbon and siamang, vol 1. Karger, Basel, pp 1–89
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: 213–237
Hall LM, Jones D, Wood B (1996) Evolutionary relationships between gibbon subgenera inferred from DNA sequence data. Biochem Soc Trans 24:416S
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
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 89:8611–8615
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 97:37–47
Koehler U, Bigoni F, Wienberg J, Stanyon R (1995b) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287–292
Marks J (1982) Evolutionary tempo and phylogenetic inference based on primate karyotypes. Cytogenet Cell Genet 34:261–264
Müller S, Wienberg J (2001) "Bar-coding" primate chromosomes: molecular cytogenetic screening for the ancestral hominoid karyotype. Hum Genet 109:85–94
Müller S, O'Brien PC, Ferguson-Smith MA, Wienberg J (1998) Cross-species colour segmenting: a novel tool in human karyotype analysis. Cytometry 33:445–452
Müller S, Neusser M, Wienberg J (2002) Towards unlimited colors for fluorescence in-situ hybridization (FISH). Chromosome Res 10:223–232
Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, London
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 92:248–253
Prouty LA, Buchanan PD, Pollitzer WS, Mootnick AR (1983) A presumptive new hylobatid subgenus with 38 chromosomes. Cytogenet Cell Genet 35:141–142
Rokas A, Holland WH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459
Roos C, Geissmann T (2001) Molecular phylogeny of the major hylobatid divisions. Mol Phylogenet Evol 19:486–494
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 273:494–497
Speicher MR, Gwyn Ballard S, Ward DC (1996) Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nat Genet 12:368–375
Stanyon R, Chiarelli B (1983) Mode and tempo in primate chromosomal evolution: implications for hylobatid phylogeny. J Hum Evol 10:305–315
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) 48:56–64
Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4th edn. Sinauer Associates, Sunderland, Mass.
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 4:257–263
Turleau C, Creau-Goldberg N, Cochet C, Grouchy J de (1983) Gene mapping of the gibbon. Its position in primate evolution. Hum Genet 64:65–72
Van Tuinen P, Ledbetter DH (1983) Cytogenetic comparison and phylogeny of three species of Hylobatidae. Am J Phys Anthropol 61:453–466
Van Tuinen P, Ledbetter DH (1989) New confirmatory and regional gene assignments in the white-cheeked gibbon Hylobates concolor. Cytogenet Cell Genet 51:1094–1095
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 110:129–142
Wienberg J, Jauch A, Stanyon R, Cremer T (1990) Molecular cytotaxonomy of primates by chromosomal in situ suppression hybridization. Genomics 8:347–350
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 101:265–270
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 207–244
Wurster DH, Benirschke K (1969) Chromosomes of some primates. Mamm Chromosome Newsletter 10:3
Yu D, Yang F, Liu R (1997) A comparative chromosome map between human and Hylobates hoolock built by chromosome painting. Yi Chuan Xue Bao 24:417–423
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This work was funded by the Deutsche Forschungsgemeinschaft (DFG Wi 970/6–1).
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Müller, S., Hollatz, M. & Wienberg, J. Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113, 493–501 (2003). https://doi.org/10.1007/s00439-003-0997-2
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DOI: https://doi.org/10.1007/s00439-003-0997-2