Advertisement

Human Genetics

, Volume 122, Issue 5, pp 477–483 | Cite as

A most distant intergeneric hybrid offspring (Larcon) of lesser apes, Nomascus leucogenys and Hylobates lar

  • Hirohisa Hirai
  • Yuriko Hirai
  • Hiroshi Domae
  • Yoko Kirihara
Original Investigation

Abstract

Unlike humans, which are the sole remaining representatives of a once larger group of bipedal apes (hominins), the “lesser apes” (hylobatids) are a diverse radiation with numerous extant species. Consequently, the lesser apes can provide a valuable evolutionary window onto the possible interactions (e.g., interbreeding) of hominin lineages coexisting in the same time and place. In the present work, we employ chromosomal analyses to verify the hybrid ancestry of an individual (Larcon) produced by two of the most distant genera of lesser apes, Hylobates (lar-group gibbons) and Nomascus (concolor-group gibbons). In addition to a mixed pelage pattern, the hybrid animal carries a 48-chromosome karyotype that consists of the haploid complements of each parental species: Hylobates lar (n = 22) and Nomascus leucogenys leucogenys (n = 26). Studies of this animal’s karyotype shed light onto the processes of speciation and genus-level divergence in the lesser apes and, by extension, across the Hominoidea.

Keywords

Chromosome Painting Hybrid Offspring Nucleolar Dominance Cheek Patch Pelage Pattern 
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.

Notes

Acknowledgments

We thank C. P. Groves for his valuable comments to the manuscript and A. Tosi for his critical reading and revising of the manuscript. This study was supported by the twenty-first century COE (A14) and the Global COE (A06).

References

  1. Brandon-Jones D, Eudey AA, Geissmann T, Groves CP, Melnick DJ, Morales JC, Shekelle M, Stewart C-B (2004) Asian primate classification. Int J Primatol 25:97–163CrossRefGoogle Scholar
  2. Brockelman WY, Gittins SP (1984) Natural hybridization in the Hylobates lar species group: implications for speciation in gibbons. In: Preushoft H, Chivers DJ, Brockelman WY, Creel N (eds) The lesser apes. Edinburgh University Press, Edinburgh, pp 498–532Google Scholar
  3. Carbone L, Vessere GM, ten Hallers BFH, Zhu B, Osoegawa K, Mootnick A, Kofler A, Wienberg J, Rogers J, Humphray S, Scott C, Harris RA, Milosavljevic A, de Jong PJ (2006) A high-resolution map of synteny disruptions in gibbon and human genomes. PLos Genet 2:e223PubMedCrossRefGoogle Scholar
  4. Chiarelli B (1972) The karyotypes of the gibbons. In: Rumbaugh DM (ed) Gibbon and Siamang, vol 1. Karger, Basel, pp 90–102Google Scholar
  5. Couturier J, Lernould J-M (1991) Karyotypic study of four gibbon forms provisionally considered as subspecies of Hylobates (Nomascus) concolor (Primates, Hylobatidae). Folia Primatol 56:95–104PubMedGoogle Scholar
  6. Disotell TR (2006) ‘Chumanzee’ evolution: the urge to diverge and merge. Genome Biol 7:240PubMedCrossRefGoogle Scholar
  7. Dunbar RIM, Dunbar P (1973) On hybridization between Theropithecus gelada and Papio anubis in the wild. J Hum Evol 3:187–192CrossRefGoogle Scholar
  8. Geissmann T (2002) Duet-splitting and the evolution of gibbon songs. Biol Rev 77:57–76PubMedGoogle Scholar
  9. Groves CP (1972) Systematics and phylogeny of gibbons. In: Rumbaugh DM (ed) Gibbon and Siamang, vol 1. Karger, Basel, pp 1–89Google Scholar
  10. Groves C (2001) Primate taxonomy. Smithonian Institution Press, WashingtonGoogle Scholar
  11. Guillen AKZ, Hirai Y, Tanoue T, Hirai H (2004) Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chrom Res 12:225–237PubMedCrossRefGoogle Scholar
  12. Hall LM, Jones DS, Wood BA (1998) Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. Mol Phylogenet Evol 10:281–286PubMedCrossRefGoogle Scholar
  13. Hayashi S, Hayasaka K, Takenaka O, Horai S (1995) Molecular phylogeny of gibbons inferred from mitochondrial DNAsequences: preliminary report. J Mol Evol 41:359–365PubMedCrossRefGoogle Scholar
  14. Hirai H, Taguchi T, Godwin AK (1999) Genomic differentiation of 18S ribosomal DNA and β-satellite DNA in the hominoid and its evolutionary aspects. Chrom Res 7:531–540PubMedCrossRefGoogle Scholar
  15. Hirai H, Mootnick AR, Takenaka O, Suryobroto B, Mouri T, Kawamoto Y, Katoh A, Kimura N, Katoh A, Maeda N (2003) Genetic mechanism and property of a whole-arm translocation (WAT) between chromosomes 8 and 9 of agile gibbons (Hylobates agilis). Chrom Res 11:37–50PubMedCrossRefGoogle Scholar
  16. Hirai H, Wijayanto H, Tanaka H, Mootnick AR, Hayano A, Perwitasari-Frajalla D, Iskandariati D, Sajuthi D (2005) A whole-arm translocation (WAT8/9) separating Sumatran and Bornean agile gibbons, and its evolutionary features. Chrom Res 13:123–133PubMedCrossRefGoogle Scholar
  17. 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 89:8611–8615PubMedCrossRefGoogle Scholar
  18. Koehler U, Bigoni F, Wienberg J, Stanyon R (1995) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287–292PubMedCrossRefGoogle Scholar
  19. Kopp E, Mayr B, Schleger W (1986) Species-specific non-expression of ribosomal RNA genes in a mammalian hybrid, the mule. Chromosoma 94:346–352PubMedCrossRefGoogle Scholar
  20. Marshall J, Sugardjito J (1986) Gibbon systematics. In: Swindler DR, Erwin J (eds) Comparative primate biology, vol 1, systematics, evolution, and anatomy. Alan R. Liss, New York, pp 137–185Google Scholar
  21. Moore CM, Janish C, Eddy CA, Hubbard CB, Leland MM, Rogers J (1999) Cytogenetic and fertility studies of a Rheboon, Rhesus macaque (Macaca mulatta) × Babboon (Papio hamadryas) cross: further support for a single karyotype nomenclature. Am J Physic Anthropol 110:119–127CrossRefGoogle Scholar
  22. Mootnick A, Groves C (2005) A new generic name for the hoolock gibbon (Hylobates). Int J Primatol 26:971–976CrossRefGoogle Scholar
  23. Müller S, Hollatz M, Weinberg J (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113:493–501PubMedCrossRefGoogle Scholar
  24. Myers RH, Shafer DA (1979) Hybrid ape offspring of a mating of gibbon and siamang. Science 205:308–310PubMedCrossRefGoogle Scholar
  25. Neusser M, Munch M, Anzenberger G, Müller S (2005) Investigation of marmoset hybrids (Cebuella pygmaea × Callithrix jacchus) and related Callitrichinae (Platyrrhini) by cross-species chromosome painting and comparative genomic hybridization. Cytogenet Genome Res 108:191–196PubMedCrossRefGoogle Scholar
  26. O’Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Weinberg J, Stanyon R, Copeland NG, Jenkins NA, Womack J, Marshall JA, Graves JM (1999) The promise of comparative genomics in mammals. Science 286:458–481PubMedCrossRefGoogle Scholar
  27. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103–1108PubMedCrossRefGoogle Scholar
  28. Pikaard CS (2000) The epigenetics of nucleolar dominance. Trends Genet 16:495–500PubMedCrossRefGoogle Scholar
  29. Primate Research Institute, Kyoto University (2002) Guide for the Care and Use of Laboratory Primates, 2nd edn. Primate Research Institute, Kyoto University, InuyamaGoogle Scholar
  30. Prouty LA, Buchanan PD, Pollitzer WS, Mootnick AR (1983) A presumptive new hylobatid subgenus with 38 chromosomes. Cytogenet Cell Genet 35:141–142PubMedGoogle Scholar
  31. Reeder RH (1985) Mechanisms of nucleolar dominace in animals and plants. J Cell Biol 101:2013–2016PubMedCrossRefGoogle Scholar
  32. Roberto R, Capozzi O, Wilson RK, Mardis ER, Lomiento M, Tuzun E, Cheng Z, Mootnick AR, Archidiacono N, Rocchi M, Eichler EE (2007) Molecular refinement of gibbon genome rearrangements. Genome Res 17:249–257PubMedCrossRefGoogle Scholar
  33. Roos C, Geissmann T (2001) Molecular phylogeny of the major hylobatid divisions. Mol Phyl Evol 19:486–494CrossRefGoogle Scholar
  34. Stanyon R, Fantini C, Camperio-Ciani C, Chiarelli B, Ardito G (1988) Banded karyotypes of 20 Papionini species reveal no necessary correlation with speciation. Am J Primatol 16:3–17CrossRefGoogle Scholar
  35. Sumner AT (1972) A simple technique for demonstrating centromere heterochromatin. Exp Cell Res 75:304–306PubMedCrossRefGoogle Scholar
  36. The Zoological Society of London (1970) Species of wild animals bred captivity during 1968. International Zoo Yearbook, vol 10, p 257Google Scholar
  37. van Gelder RG (1977) Mammalian hybrids and generic limits. Am Museum Novitates 2635:1–25Google Scholar
  38. van Tuinen P, Ledbetter DH (1983) Cytogenetic comparison and phylogeny of the species of Hylobatidae. Am J Phys Anthropol 61:453–466PubMedCrossRefGoogle Scholar
  39. Wijayanto H, Hirai Y, Kamanaka Y, Katho A, Sajuthi D, Hirai H (2005) Patterns of C-heterochromatin and telomeric DNA in two representative group of small apes, the genera Hylobates and Symphalangus. Chrom Res 13:717–724PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Hirohisa Hirai
    • 1
  • Yuriko Hirai
    • 1
  • Hiroshi Domae
    • 2
  • Yoko Kirihara
    • 2
  1. 1.Primate Research InstituteKyoto UniversityInuyama AichiJapan
  2. 2.Ishikawa ZooIshikawaJapan

Personalised recommendations