Chromosomal phylogeny and evolution of gibbons (Hylobatidae)

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.

[1]  J. Garza,et al.  A phylogenetic study of the gibbons (Hylobates) using DNA obtained noninvasively from hair. , 1992, Molecular phylogenetics and evolution.

[2]  J. Napier,et al.  A Handbook of Living Primates , 1969 .

[3]  D. Ledbetter,et al.  Cytogenetic comparison and phylogeny of three species of Hylobatidae. , 1983, American journal of physical anthropology.

[4]  C. Turleau,et al.  Gene mapping of the gibbon. Its position in primate evolution , 2004, Human Genetics.

[5]  B. Chiarelli,et al.  Mode and tempo in primate chromosome evolution: Implications for hylobatid phylogeny , 1983 .

[6]  T. Geissmann Taxonomy and evolution of gibbons , 2003 .

[7]  A. Mootnick,et al.  Complex, compound inversion/translocation polymorphism in an ape: presumptive intermediate stage in the karyotypic evolution of the agile gibbon Hylobates agilis. , 1999, American journal of physical anthropology.

[8]  F. Ayala,et al.  PHYLOGENETIC RELATIONSHIPS BETWEEN MAN AND THE APES: ELECTROPHORETIC EVIDENCE , 1979, Evolution; international journal of organic evolution.

[9]  P. Holland,et al.  Rare genomic changes as a tool for phylogenetics. , 2000, Trends in ecology & evolution.

[10]  J. Wienberg,et al.  Insights into Mammalian Genome Organization and Evolution by Molecular Cytogenetics , 2000 .

[11]  D. Chivers,et al.  A phylogeny of gibbons (Hylobates spp.) based on morphological and behavioural characters. , 1982, Folia primatologica; international journal of primatology.

[12]  A. Jauch,et al.  Homologies in human and Macasa fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries , 2004, Chromosoma.

[13]  H. R. Catchpole,et al.  A Handbook of Living Primates , 1968, The Yale Journal of Biology and Medicine.

[14]  J. Wienberg,et al.  "Bar-coding" primate chromosomes: molecular cytogenetic screening for the ancestral hominoid karyotype , 2001, Human Genetics.

[15]  A. Jauch,et al.  Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Martin,et al.  Anthropology and primatology into the third millenium: the centenary congress of the Zürich Anthropological Institute , 2002 .

[17]  A. Mootnick,et al.  A presumptive new hylobatid subgenus with 38 chromosomes. , 1983, Cytogenetics and cell genetics.

[18]  B. Dutrillaux,et al.  [Karyotype analysis of 2 species of gibbons (Hylobates lar and H. concolor) with different banding species]. , 1975, Cytogenetics and cell genetics.

[19]  M A Ferguson-Smith,et al.  Cross-species colour segmenting: a novel tool in human karyotype analysis. , 1998, Cytometry.

[20]  D Yu,et al.  [A comparative chromosome map between human and Hylobates hoolock built by chromosome painting]. , 1997, Yi chuan xue bao = Acta genetica Sinica.

[21]  J. Wienberg,et al.  Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. , 1995, Genomics.

[22]  D. Ledbetter,et al.  Multicolor Spectral Karyotyping of Human Chromosomes , 1996, Science.

[23]  L. Hall,et al.  Evolutionary relationships between gibbon subgenera inferred from DNA sequence data. , 1996, Biochemical Society transactions.

[24]  J. Wienberg,et al.  Towards unlimited colors for fluorescence in-situhybridization (FISH) , 2004, Chromosome Research.

[25]  L. Hall,et al.  Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. , 1998, Molecular phylogenetics and evolution.

[26]  A. Jauch,et al.  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. , 1996, Cytogenetics and cell genetics.

[27]  M. Bender,et al.  Chapter 7 – The Chromosomes of Primates , 1963 .

[28]  B. Dutrillaux,et al.  Analysis of the karyotype of two species of gibbons (Hylobates lar and H. concolor) by various banding techniques , 1975 .

[29]  B. Chiarelli,et al.  Banded Karyotypes of the 44-Chromosome Gibbons , 1987 .

[30]  Alan Tunnacliffe,et al.  Cytogenetic analysis by chromosome painting using dop‐pcr amplified flow‐sorted chromosomes , 1992, Genes, chromosomes & cancer.

[31]  J. Couturier,et al.  Karyotypic study of four gibbon forms provisionally considered as subspecies of Hylobates (Nomascus) concolor (Primates, Hylobatidae). , 1991, Folia primatologica; international journal of primatology.

[32]  J. Wienberg,et al.  Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization. , 1995, American journal of physical anthropology.

[33]  T. Geissmann,et al.  Molecular phylogeny of the major hylobatid divisions. , 2001, Molecular phylogenetics and evolution.

[34]  J. Marks,et al.  Evolutionary tempo and phylogenetic inference based on primate karyotypes. , 1982, Cytogenetics and cell genetics.

[35]  A. Jauch,et al.  Molecular cytotaxonomy of primates by chromosomal in situ suppression hybridization. , 1990, Genomics.

[36]  D. Ward,et al.  Karyotyping human chromosomes by combinatorial multi-fluor FISH , 1996, Nature Genetics.

[37]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .