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.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Received: September 16, 2020
  2. Accepted: February 16, 2021
  3. Accepted Manuscript published: February 18, 2021 (version 1)
  4. Version of Record published: March 15, 2021 (version 2)
  5. Version of Record updated: April 1, 2021 (version 3)

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.

Metrics

  • 2,028
    views
  • 226
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Rémi Allio
  2. Marie-Ka Tilak
  3. Celine Scornavacca
  4. Nico L Avenant
  5. Andrew C Kitchener
  6. Erwan Corre
  7. Benoit Nabholz
  8. Frédéric Delsuc
(2021)
High-quality carnivoran genomes from roadkill samples enable comparative species delineation in aardwolf and bat-eared fox
eLife 10:e63167.
https://doi.org/10.7554/eLife.63167

Share this article

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

Further reading

    1. Evolutionary Biology
    Isabella Tomanek
    Insight

    Laboratory experiments on a fluorescent protein in E. coli reveal how duplicate genes are rapidly inactivated by mutations during evolution.

    1. Evolutionary Biology
    Maryline Blin, Louis Valay ... Sylvie Rétaux
    Research Article

    Animals are adapted to their natural habitats and lifestyles. Their brains perceive the external world via their sensory systems, compute information together with that of internal states and autonomous activity, and generate appropriate behavioral outputs. However, how do these processes evolve across evolution? Here, focusing on the sense of olfaction, we have studied the evolution in olfactory sensitivity, preferences, and behavioral responses to six different food-related amino acid odors in the two eco-morphs of the fish Astyanax mexicanus. To this end, we have developed a high-throughput behavioral setup and pipeline of quantitative and qualitative behavior analysis, and we have tested 489 six-week-old Astyanax larvae. The blind, dark-adapted morphs of the species showed markedly distinct basal swimming patterns and behavioral responses to odors, higher olfactory sensitivity, and a strong preference for alanine, as compared to their river-dwelling eyed conspecifics. In addition, we discovered that fish have an individual ‘swimming personality’, and that this personality influences their capability to respond efficiently to odors and find the source. Importantly, the personality traits that favored significant responses to odors were different in surface fish and cavefish. Moreover, the responses displayed by second-generation cave × surface F2 hybrids suggested that olfactory-driven behavior and olfactory sensitivity is a quantitative genetic trait. Our findings show that olfactory processing has rapidly evolved in cavefish at several levels: detection threshold, odor preference, and foraging behavior strategy. Cavefish is therefore an outstanding model to understand the genetic, molecular, and neurophysiological basis of sensory specialization in response to environmental change.