Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
- University of Glasgow, United Kingdom
- University of Miami, United States
- 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.
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Stepwise colonization of the Andes by Ruddy Ducks and the evolution of novel β‐globin variantsGenBank AY747742-AY747751; AY747756-AY747778; AM084943-AM084997; JX910949-JX910971.
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Multilocus coalescent analysis of haemoglobin differentiation between low‐and high‐altitude populations of crested ducks (Lophonetta specularioides)GenBank HM063481-HM063503; JN833791-JN833847.
Article and author information
Author details
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.
Reviewing Editor
- Kevin Campbell, University of Manitoba, Canada
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.
Version history
- Received: February 21, 2020
- Accepted: July 23, 2020
- Accepted Manuscript published: July 30, 2020 (version 1)
- Accepted Manuscript updated: August 10, 2020 (version 2)
- Version of Record published: September 16, 2020 (version 3)
- 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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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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