1. Evolutionary Biology
Download icon

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

  1. Neal J Dawson  Is a corresponding author
  2. Luiz 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
Research Article
  • Cited 0
  • Views 575
  • Annotations
Cite this article as: eLife 2020;9:e56259 doi: 10.7554/eLife.56259

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.

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. Luiz 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.

Metrics

  • 575
    Page views
  • 107
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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

  1. Further reading

Further reading

    1. Evolutionary Biology
    Rylan Shearn et al.
    Short Report

    Sex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex-chromosome biology both from a functional and evolutionary perspective. The evolution of the pseudoautosomal boundary (PAB) is well documented in haplorrhines (apes and monkeys) but not in strepsirrhines (lemurs and lorises). Here we studied the PAB of seven species representing the main strepsirrhine lineages by sequencing a male and a female genome in each species and using sex differences in coverage to identify the PAB. We found that during primate evolution, the PAB has remained unchanged in strepsirrhines whereas several recombination suppression events moved the PAB and shortened the pseudoautosomal region in haplorrhines. Strepsirrhines are well known to have much lower sexual dimorphism than haplorrhines. We suggest that mutations with antagonistic effects between males and females have driven recombination suppression and PAB evolution in haplorrhines.

    1. Ecology
    2. Evolutionary Biology
    Susanne RK Zajitschek et al.
    Research Article

    Biomedical and clinical sciences are experiencing a renewed interest in the fact that males and females differ in many anatomic, physiological, and behavioral traits. Sex differences in trait variability, however, are yet to receive similar recognition. In medical science, mammalian females are assumed to have higher trait variability due to estrous cycles (the 'estrus-mediated variability hypothesis'); historically in biomedical research, females have been excluded for this reason. Contrastingly, evolutionary theory and associated data support the 'greater male variability hypothesis'. Here, we test these competing hypotheses in 218 traits measured in >26,900 mice, using meta-analysis methods. Neither hypothesis could universally explain patterns in trait variability. Sex-bias in variability was trait-dependent. While greater male variability was found in morphological traits, females were much more variable in immunological traits. Sex-specific variability has eco-evolutionary ramifications including sex-dependent responses to climate change, as well as statistical implications including power analysis considering sex difference in variance.