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Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla

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Abstract

The order Perissodactyla, the group of odd-toed ungulates, includes three extant families: Equidae, Tapiridae, and Rhinocerotidae. The extremely rapid karyotypic diversification in perissodactyls has so far prevented the establishment of genome-wide homology maps between these three families by traditional cytogenetic approaches. Here we report the first genome-wide comparative chromosome maps of African rhinoceroses, four tapir species, four equine species, and humans. These maps were established by multidirectional chromosome painting, with paint probes derived from flow-sorted chromosomes of Equus grevyi, Tapirus indicus, and Ceratotherium simum as well as painting probes from horse and human. The Malayan tapir (Tapirus indicus), Baird’s tapir (T. bairdii), mountain tapir (T. pinchaque), lowland tapir (T. terrestris), and onager (E. hemionus onager), were studied by cross-species chromosome painting for the first time. Our results, when integrated with previously published comparative chromosome maps of the other perissodactyl species, have enabled the reconstruction of perissodactyl, ceratomorph, and equid ancestral karyotypes, and the identification of the defining evolutionary chromosomal rearrangements along each lineage. Our results allow a more reliable estimate of the mode and tempo of evolutionary chromosomal rearrangements, revealing a striking switch between the slowly evolving ceratomorphs and extremely rapidly evolving equids.

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    Vladimir A. Trifonov, Anastasia I. Nesterenko, Polina L. Perelman, Nadezhda V. Rubtsova & Alexander S. Graphodatsky

  2. Department of Veterinary Medicine, Cambridge Resource Centre for Comparative Genomics, Cambridge, CB3 0ES, UK

    Vladimir A. Trifonov, Beiyuan Fu, Patricia C M O’Brien & Malcolm A. Ferguson-Smith

  3. Department of Animal Biology and Genetics, University of Florence, Florence, 50122, Italy

    Roscoe Stanyon

  4. National Cancer Institute, Frederick, MD, 21702, USA

    Polina L. Perelman & Gary Stone

  5. Conservation and Research for Endangered Species, Zoological Society of San Diego, San Diego, CA, USA

    Marlys L. Houck

  6. Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Matieland, South Africa

    Terence J. Robinson

  7. Institut de Recherche pour le Développement, Centre de Biologie et Gestion des Populations, Campus International de Baillarguet, CS30016, 34988, Montferrier-sur-Lez, France

    Gauthier Dobigny

  8. The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

    Fengtang Yang

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  1. Vladimir A. Trifonov
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  2. Roscoe Stanyon
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  3. Anastasia I. Nesterenko
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  4. Beiyuan Fu
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  5. Polina L. Perelman
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  6. Patricia C M O’Brien
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  7. Gary Stone
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  8. Nadezhda V. Rubtsova
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  9. Marlys L. Houck
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  10. Terence J. Robinson
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  11. Malcolm A. Ferguson-Smith
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  12. Gauthier Dobigny
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  13. Alexander S. Graphodatsky
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  14. Fengtang Yang
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Corresponding authors

Correspondence to Vladimir A. Trifonov or Fengtang Yang.

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Supplementary Table S1

Matrix of human-based (HSA) and horse-based (ECA) chromosomal characters. EPR, EHE, EAS, EZE, EGR, EBU, CSI, DBI, TIN, TBA, TTE, TPI represent Przewalski’s horse, onager, donkey, mountain zebra, Grevy’s zebra, Burchell’s zebra, white rhinoceros, black rhinoceros, Malayan tapir, Baird’s tapir, lowland tapir, and mountain tapir respectively. Partial chromosomes/chromosome arms are marked by inverted commas. “Inv” indicates inversion (DOC 154 kb)

Supplementary Figure S2

Karyotype of Grevy’s zebra with human (HSA) and Malayan tapir (TIN) homologies. Human homologies that were not found in these experiments, but are inferred from previously published data are indicated by circles (JPEG 214 kb)

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Trifonov, V.A., Stanyon, R., Nesterenko, A.I. et al. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Res 16, 89–107 (2008). https://doi.org/10.1007/s10577-007-1201-7

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