High-quality carnivoran genomes from roadkill samples enable comparative species delineation in aardwolf and bat-eared fox

  1. Rémi Allio  Is a corresponding author
  2. Marie-Ka Tilak
  3. Celine Scornavacca
  4. Nico L Avenant
  5. Andrew C Kitchener
  6. Erwan Corre
  7. Benoit Nabholz
  8. Frédéric Delsuc  Is a corresponding author
  1. CNRS, IRD, EPHE, Université de Montpellier, France
  2. National Museum and Centre for Environmental Management, University of the Free State, Bloemfontein, South Africa, France
  3. National Museums Scotland, United Kingdom
  4. CNRS, Sorbonne Université, FR2424, ABiMS, Station Biologique de Roscoff, 29680 Roscoff, France, France
  5. UMR 5554 ISEM (Université de Montpellier-CNRS-IRD-EPHE), France
  6. CNRS - Université de Montpellier, France

Abstract

In a context of ongoing biodiversity erosion, obtaining genomic resources from wildlife is essential for conservation. The thousands of yearly mammalian roadkill provide a useful source material for genomic surveys. To illustrate the potential of this underexploited resource, we used roadkill samples to study the genomic diversity of the bat-eared fox (Otocyon megalotis) and the aardwolf (Proteles cristatus), both having subspecies with similar disjunct distributions in Eastern and Southern Africa. First, we obtained reference genomes with high contiguity and gene completeness by combining Nanopore long reads and Illumina short reads. Then, we showed that the two subspecies of aardwolf might warrant species status (P. cristatus and P. septentrionalis) by comparing their genome-wide genetic differentiation to pairs of well-defined species across Carnivora with a new Genetic Differentiation index (GDi) based on only a few resequenced individuals. Finally, we obtained a genome-scale Carnivora phylogeny including the new aardwolf species.

Data availability

Genome assemblies, associated Illumina and Nanopore sequence reads, and mitogenomes have been submitted to the National Center for Biotechnology Information (NCBI) and will be available after publication under BioProject number PRJNA681015. The full analytical pipeline, phylogenetic datasets (mitogenomic and genomic), corresponding trees, and other supplementary materials are available from zenodo.org (DOI: 10.5281/zenodo.4479226).

The following data sets were generated
The following previously published data sets were used
    1. Liu S
    2. Lorenzen ED
    3. Fumagalli M
    4. Li B
    5. Harris K
    6. Xiong Z
    7. Zhou L
    8. Korneliussen TS
    9. Somel M
    10. Babbitt C
    11. et al.
    (2014) Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears.
    PB43 : SRR942203, SRR942290, SRR942298; PB28: SRR942211, SRR942287, SRR942295; Brown Bear: SRR935591, SRR935625, SRR935627.

Article and author information

Author details

  1. Rémi Allio

    Institut des Sciences de l Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France
    For correspondence
    rem.allio@yahoo.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3885-5410
  2. Marie-Ka Tilak

    Institut des Sciences de l Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Celine Scornavacca

    Institut des Sciences de l Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, France, CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Nico L Avenant

    Department of Mammalogy, National Museum and Centre for Environmental Management, University of the Free State, Bloemfontein, South Africa, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Andrew C Kitchener

    Department of Natural Sciences, National Museums Scotland, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Erwan Corre

    Informatics and Bioinformatics, CNRS, Sorbonne Université, FR2424, ABiMS, Station Biologique de Roscoff, 29680 Roscoff, France, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Benoit Nabholz

    UMR 5554 ISEM (Université de Montpellier-CNRS-IRD-EPHE), Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Frédéric Delsuc

    Institut des Sciences de l'Evolution, CNRS - Université de Montpellier, Montpellier, France
    For correspondence
    frederic.delsuc@umontpellier.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6501-6287

Funding

H2020 European Research Council (ERC‐2015‐CoG‐683257)

  • Frédéric Delsuc

Agence Nationale de la Recherche (ANR‐10‐LABX‐25‐01)

  • Rémi Allio
  • Marie-Ka Tilak
  • Celine Scornavacca
  • Benoit Nabholz
  • Frédéric Delsuc

Agence Nationale de la Recherche (ANR‐10‐LABX‐0004)

  • Rémi Allio
  • Marie-Ka Tilak
  • Celine Scornavacca
  • Benoit Nabholz
  • Frédéric Delsuc

Agence Nationale de la Recherche (ANR-11-INBS-0013)

  • Erwan Corre

National Research Foundation (86321)

  • Nico L Avenant

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Allio et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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https://doi.org/10.7554/eLife.63167

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