Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl

  1. Neal J Dawson  Is a corresponding author
  2. Luis Alza
  3. Gabriele Nandal
  4. Graham R Scott
  5. Kevin G McCracken
  1. University of Glasgow, United Kingdom
  2. University of Miami, United States
  3. McMaster University, Canada

Abstract

High-altitude environments require that animals meet the metabolic O2 demands for locomotion and thermogenesis in O2-thin air, but the degree to which convergent metabolic changes have arisen across independent high-altitude lineages or the speed at which such changes arise is unclear. We examined seven high-altitude waterfowl that have inhabited the Andes (3812-4806m elevation) over varying evolutionary time scales, to elucidate changes in biochemical pathways of energy metabolism in flight muscle relative to low-altitude sister-taxa. Convergent changes across high-altitude taxa included increased hydroxyacyl-coA dehydrogenase and succinate dehydrogenase activities, decreased lactate dehydrogenase, pyruvate kinase, creatine kinase, and cytochrome c oxidase activities, and increased myoglobin content. ATP synthase activity increased in only the longest established high-altitude taxa, whereas hexokinase activity increased in only newly established taxa. Therefore, changes in pathways of lipid oxidation, glycolysis, and mitochondrial oxidative phosphorylation are common strategies to cope with high-altitude hypoxia, but some changes require longer evolutionary time to arise.

Data availability

- Mitochondrial DNA sequences for Anas puna and Anas versicolor were deposited in GenBank under accession numbers MN734269-MN734345.- All data generated or analysed during this study are included in the manuscript and supporting files.

The following previously published data sets were used

Article and author information

Author details

  1. Neal J Dawson

    Institute of Biodiversity Animal Health & Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
    For correspondence
    neal.dawson@glasgow.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5389-8692
  2. Luis Alza

    Biology, University of Miami, Coral Gables, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Gabriele Nandal

    Biology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Graham R Scott

    Biology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4225-7475
  5. Kevin G McCracken

    Biology, University of Miami, Coral Gables, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Natural Sciences and Engineering Research Council of Canada (Discovery Grant)

  • Graham R Scott

National Science Foundation (IOS-0949439)

  • Kevin G McCracken

Canadian Foundation for Innovation (John R. Evans Leaders Fund)

  • Graham R Scott

Ontario Ministry of Research and Innovation (Early Researcher Award)

  • Graham R Scott

Kushlan Endowment for Waterbird Biology and Conservation (Kushlan Chair)

  • Kevin G McCracken

Canada Research Chairs (Tier 2 - Comparative and Environmental Physiology)

  • Graham R Scott

Natural Sciences and Engineering Research Council of Canada (Postdoctoral Fellowship)

  • Neal J Dawson

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

Ethics

Animal experimentation: Samples were imported to Canada with authorization from the Canadian Wildlife Service (Scientific Possession No. 369) and collected with authorization from the Servicio Nacional de Area Naturales Protegidas del Peru (004-2014-SERNANP-DGANP-RNT/J), Dirección General Forestal y de Fauna Silvestre del Peru (RD 169-2014-MIN AGRI-DGFFS/DGEFFS, 190-2015-SERFOR-DGGSPFFS), Ministerio de Industria, Agricultura, y Ganaderia Chubut (No. 24/07 y 1636/14), Ministerio de Asuntos Agrarios Buenos Aires , Oregon Department of Fish and Wildlife (101-15), and USFWS Region 1 Migratory Bird Permit Office (MB68890B-0). All protocols were carried out in accordance with guidelines that were approved by the institutional animal care and use committee at the University of Miami or University of Alaska.

Reviewing Editor

  1. Kevin Campbell, University of Manitoba, Canada

Publication history

  1. Received: February 21, 2020
  2. Accepted: July 23, 2020
  3. Accepted Manuscript published: July 30, 2020 (version 1)
  4. Accepted Manuscript updated: August 10, 2020 (version 2)
  5. Version of Record published: September 16, 2020 (version 3)
  6. Version of Record updated: September 17, 2020 (version 4)

Copyright

© 2020, Dawson 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. Neal J Dawson
  2. Luis Alza
  3. Gabriele Nandal
  4. Graham R Scott
  5. Kevin G McCracken
(2020)
Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
eLife 9:e56259.
https://doi.org/10.7554/eLife.56259

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