Structural variations of subterminal satellite blocks and their source mechanisms as inferred from the meiotic configurations of chimpanzee chromosome termini

  • Hirohisa HiraiEmail author
  • Yuriko Hirai
  • Toshifumi Udono
  • Kiyoaki Matsubayashi
  • Anthony J. Tosi
  • Akihiko Koga
Original Article


African great apes have large constitutive heterochromatin (C-band) blocks in subtelomeric regions of the majority of their chromosomes, but humans lack these. Additionally, the chimpanzee meiotic cell division process demonstrates unique partial terminal associations in the first meiotic prophase (pachytene). These are likely formed as a result of interaction among subtelomeric C-band blocks. We thus conducted an extensive study to define the features in the subtelomeric heterochromatic regions of chimpanzee chromosomes undergoing mitotic metaphase and meiotic cell division. Molecular cytogenetic analyses with probes of both subterminal satellite DNA (a main component of C-band) and rDNA demonstrated principles of interaction among DNA arrays. The results suggest that homologous and ectopic recombination through persistent subtelomeric associations (post-bouquet association observed in 32% of spermatocytes in the pachytene stage) appears to create variability in heterochromatin patterns and simultaneously restrain subtelomeric genome polymorphisms. That is, the meeting of non-homologous chromosome termini sets the stage for ectopic pairing which, in turn, is the mechanism for generating variability and genomic dispersion of subtelomeric C-band blocks through a system of concerted evolution. Comparison between the present study and previous reports indicated that the chromosomal distribution rate of sutelomeric regions seems to have antagonistic correlation with arm numbers holding subterminal satellite blocks in humans, chimpanzees, and gorillas. That is, the increase of subterminal satellite blocks probably reduces genomic diversity in the subtelomeric regions. The acquisition vs. loss of the subtelomeric C-band blocks is postulated as the underlying engine of this chromosomal differentiation yielded by meiotic chromosomal interaction.


constitutive heterochromatin repeat array association concerted evolution interchromosomal recombination 



Constitutive heterochromatin


Centromeric C-band




Fluorescent in situ hybridization


NOR-adjoining C-band


Nucleolus organizer region


Subterminal constitutive heterochromatin block


Subterminal C-band


Subterminal satellite



We thank the staff members of the Center of Human Evolution Modeling Research, Primate Research Institute, and the Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, for their technical assistance. We are grateful to the Japan Monkey Center and Ishikawa Zoo for supplying blood samples of bonobo and gorilla, respectively.

Funding information

This research was supported by grants from the Japan Society for the Promotion of Science (JSPS; 15H04427 to AK, 20405016 and 22247037 to HH), the Global Center of Excellence of the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT; Program A06, Kyoto University), the Unit of Human-Nature Interlaced Life Science, Kyoto University Research Coordination Alliance, and the Kyoto University Foundation.

Compliance with ethical standards

Animal ethics approval was obtained from the Monkey Care and Use Committee of Primate Research Institute, Kyoto University (approvals 07–1632, 08–1703, 09–1787, 2010–084).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10577_2019_9615_MOESM1_ESM.docx (31 kb)
ESM 1 (DOCX 30 kb)


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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Hirohisa Hirai
    • 1
    • 2
    Email author
  • Yuriko Hirai
    • 1
  • Toshifumi Udono
    • 3
  • Kiyoaki Matsubayashi
    • 1
  • Anthony J. Tosi
    • 4
  • Akihiko Koga
    • 1
  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.The Unit of Human-Nature Interlaced Life ScienceKyoto University Research Coordination AllianceKyotoJapan
  3. 3.Kumamoto Sanctuary, Wildlife Research CenterKyoto UniversityUtoJapan
  4. 4.Department of Anthropology and School of Biomedical ScienceKent State UniversityKentUSA

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