Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers

  1. Kai He  Is a corresponding author
  2. Triston G Eastman
  3. Hannah Czolacz
  4. Shuhao Li
  5. Akio Shinohara
  6. Shin-ichiro Kawada
  7. Mark S Springer
  8. Michael Berenbrink  Is a corresponding author
  9. Kevin L Campbell  Is a corresponding author
  1. Southern Medical University, China
  2. University of Manitoba, Canada
  3. University of Liverpool, United Kingdom
  4. University of Miyazaki, Japan
  5. National Museum of Nature and Science, Japan
  6. University of California, Riverside, United States

Abstract

The speciose mammalian order Eulipotyphla (moles, shrews, hedgehogs, solenodons) combines an unusual diversity of semi-aquatic, semi-fossorial, and fossorial forms that arose from terrestrial forbearers. However, our understanding of the ecomorphological pathways leading to these lifestyles has been confounded by a fragmentary fossil record, unresolved phylogenetic relationships, and potential morphological convergence, calling for novel approaches. The net surface charge of the oxygen-storing muscle protein myoglobin (ZMb), which can be readily determined from its primary structure, provides an objective target to address this question due to mechanistic linkages with myoglobin concentration. Here we generate a comprehensive 71 species molecular phylogeny that resolves previously intractable intra-family relationships and then ancestrally reconstruct ZMb evolution to identify ancient lifestyle transitions based on protein sequence alone. Our phylogenetically informed analyses confidently resolve fossorial habits having evolved twice in talpid moles and reveal five independent secondary aquatic transitions in the order housing the world's smallest endothermic divers.

Data availability

The newly obtained myoglobin sequences were deposited to GenBank under accession numbers MW456061 to MW456069 and MW473727- MW473769, and sequence alignments per gene were deposited to Dryad Digital Repository at https://doi.org/10.5061/dryad.brv15dv7q.

Article and author information

Author details

  1. Kai He

    School of Basic Medical Science, Southern Medical University, Guagnzhou, China
    For correspondence
    hk200131060071@163.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6234-2589
  2. Triston G Eastman

    Department of Biological Sciences, University of Manitoba, Winnipeg, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Hannah Czolacz

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Shuhao Li

    Department of Biological Sciences, University of Manitoba, Winnipeg, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Akio Shinohara

    Department of Bio-resources, University of Miyazaki, Miyazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Shin-ichiro Kawada

    Department of Zoology, National Museum of Nature and Science, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Mark S Springer

    7Department of Evolution, Ecology, and Organismal Biology, University of California, Riverside, Riverside, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Berenbrink

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    For correspondence
    Michael.Berenbrink@liverpool.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  9. Kevin L Campbell

    Department of Biological Sciences, University of Manitoba, Winnipeg, Canada
    For correspondence
    kevin.campbell@umanitoba.ca
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Natural Science Foundation of China (31970389)

  • Kai He

National Natural Science Foundation of China (31301869)

  • Kai He

National Science Foundation (DEB-1457735)

  • Mark S Springer

University of Manitoba (41342)

  • Kevin L Campbell

Natural Sciences and Engineering Research Council of Canada (RGPIN/238838-2011)

  • Kevin L Campbell

Natural Sciences and Engineering Research Council of Canada (RGPIN/6562-2016)

  • Kevin L Campbell

Natural Sciences and Engineering Research Council of Canada (RGPIN/412336-2011)

  • Kevin L Campbell

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

Reviewing Editor

  1. Shigehiro Kuraku, National Institute of Genetics, Japan

Publication history

  1. Received: January 22, 2021
  2. Accepted: May 4, 2021
  3. Accepted Manuscript published: May 5, 2021 (version 1)
  4. Version of Record published: June 15, 2021 (version 2)
  5. Version of Record updated: June 15, 2021 (version 3)
  6. Version of Record updated: June 16, 2021 (version 4)

Copyright

© 2021, He 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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  1. Kai He
  2. Triston G Eastman
  3. Hannah Czolacz
  4. Shuhao Li
  5. Akio Shinohara
  6. Shin-ichiro Kawada
  7. Mark S Springer
  8. Michael Berenbrink
  9. Kevin L Campbell
(2021)
Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers
eLife 10:e66797.
https://doi.org/10.7554/eLife.66797

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