, Volume 69, Issue 10, pp 677–688 | Cite as

Limited MHC class I intron 2 repertoire variation in bonobos

  • Natasja G. de GrootEmail author
  • Corrine M. C. Heijmans
  • Philippe Helsen
  • Nel Otting
  • Zjef Pereboom
  • Jeroen M. G. Stevens
  • Ronald E. Bontrop
Original Article


Common chimpanzees (Pan troglodytes) experienced a selective sweep, probably caused by a SIV-like virus, which targeted their MHC class I repertoire. Based on MHC class I intron 2 data analyses, this selective sweep took place about 2–3 million years ago. As a consequence, common chimpanzees have a skewed MHC class I repertoire that is enriched for allotypes that are able to recognise conserved regions of the SIV proteome. The bonobo (Pan paniscus) shared an ancestor with common chimpanzees approximately 1.5 to 2 million years ago. To investigate whether the signature of this selective sweep is also detectable in bonobos, the MHC class I gene repertoire of two bonobo panels comprising in total 29 animals was investigated by Sanger sequencing. We identified 14 Papa-A, 20 Papa-B and 11 Papa-C alleles, of which eight, five and eight alleles, respectively, have not been reported previously. Within this pool of MHC class I variation, we recovered only 2 Papa-A, 3 Papa-B and 6 Papa-C intron 2 sequences. As compared to humans, bonobos appear to have an even more diminished MHC class I intron 2 lineage repertoire than common chimpanzees. This supports the notion that the selective sweep may have predated the speciation of common chimpanzees and bonobos. The further reduction of the MHC class I intron 2 lineage repertoire observed in bonobos as compared to the common chimpanzee may be explained by a founding effect or other subsequent selective processes.


Pan paniscus Pan troglodytes mtDNA MHC Selective sweep 



We thank D. Devine for editing the manuscript and F. van Hassel for preparing the figures. This study was supported by the Biomedical Primate Research Centre.

Supplementary material

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Supplementary Fig 1

A) Information on the founder bonobos and their offspring of the EEP (European Endangered Species Programme) cohort. Names in boldface indicate the bonobos analysed for their MHC-A, -B, and -C variation. WB means wild born. *Zorba is a potential founder, as it has not generated offspring. #Yala is a child of Margrit. Seq. id stands for sequence identification, and different numbers identify unique mtDNA sequences. Acc. nr. means accession number. In the last column, the accession numbers extracted from Lobon et al. (2016) are given. For Kombote the Seq. id 6-like is given based on a comparison of the partial mtDNA D-loop sequence, but we cannot exclude the possibility that variation is present in the complete sequence. Nd means not determined. B) Overview of the mtDNA information relating to the additional bonobo panel. Names in boldface indicate the bonobos analysed for their MHC-A, -B, and -C variation. Seq. id stands for sequence identification, and nd means not determined. (JPEG 5890 kb)

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High Resolution Image (EPS 3428 kb)
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Supplementary Fig. 2

Phylogenetic analysis of exon 2 and 3 sequences for the Papa-A, -B, and -C alleles identified in the two panels. Representative human and common chimpanzee sequences were incorporated into the analysis (Maccari et al. 2017; Robinson et al. 2015). Relevant bootstrap values are indicated. (JPEG 3305 kb)

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High Resolution Image (EPS 2421 kb)
251_2017_1010_Fig8_ESM.jpg (3 mb)
Supplementary Fig. 3

Phylogenetic analysis of the Papa-A, -B, and -C intron 2 sequences identified in the two panels. Representative human and common chimpanzee sequences were incorporated into the analysis. Brackets indicate the classification into different intron 2 lineages that were previously used for classification of human and common chimpanzee samples (de Groot et al. 2002). Relevant bootstrap values are indicated. (JPEG 3051 kb)

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High Resolution Image (EPS 2427 kb)


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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Natasja G. de Groot
    • 1
    Email author
  • Corrine M. C. Heijmans
    • 1
  • Philippe Helsen
    • 2
  • Nel Otting
    • 1
  • Zjef Pereboom
    • 2
  • Jeroen M. G. Stevens
    • 2
    • 3
  • Ronald E. Bontrop
    • 1
    • 4
  1. 1.Biomedical Primate Research Centre, Department of Comparative Genetics & RefinementRijswijkThe Netherlands
  2. 2.Centre for Research and Conservation, Royal Zoological Society of AntwerpAntwerpBelgium
  3. 3.Department of BiologyUniversity of AntwerpAntwerpBelgium
  4. 4.Department of Theoretical Biology and BioinformaticsUtrecht UniversityUtrechtThe Netherlands

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