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

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 s...

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Main Authors: Neal J Dawson, Luis Alza, Gabriele Nandal, Graham R Scott, Kevin G McCracken
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/56259
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author Neal J Dawson
Luis Alza
Gabriele Nandal
Graham R Scott
Kevin G McCracken
author_facet Neal J Dawson
Luis Alza
Gabriele Nandal
Graham R Scott
Kevin G McCracken
author_sort Neal J Dawson
collection DOAJ
description 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 (3812–4806 m 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.
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spelling doaj.art-794e9188d0404fd48dfdbf6c1c989f202022-12-22T03:33:46ZengeLife Sciences Publications LtdeLife2050-084X2020-07-01910.7554/eLife.56259Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowlNeal J Dawson0https://orcid.org/0000-0001-5389-8692Luis Alza1Gabriele Nandal2Graham R Scott3https://orcid.org/0000-0002-4225-7475Kevin G McCracken4Department of Biology, McMaster University, Hamilton, Canada; Department of Biology University of Miami, Coral Gables, United StatesDepartment of Biology University of Miami, Coral Gables, United States; University of Alaska Museum and Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States; Centro de Ornitología y Biodiversidad - CORBIDI, Lima, PeruDepartment of Biology, McMaster University, Hamilton, CanadaDepartment of Biology, McMaster University, Hamilton, CanadaDepartment of Biology University of Miami, Coral Gables, United States; University of Alaska Museum and Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, United States; Centro de Ornitología y Biodiversidad - CORBIDI, Lima, Peru; Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, United States; Human Genetics and Genomics, Hussman Institute for Human Genomics, University of Miami Miller School of Medicine, Miami, United StatesHigh-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 (3812–4806 m 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.https://elifesciences.org/articles/56259birdshigh-altitude adaptationhypoxiaenergy metabolismmyoglobinmuscle energetics
spellingShingle Neal J Dawson
Luis Alza
Gabriele Nandal
Graham R Scott
Kevin G McCracken
Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
eLife
birds
high-altitude adaptation
hypoxia
energy metabolism
myoglobin
muscle energetics
title Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
title_full Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
title_fullStr Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
title_full_unstemmed Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
title_short Convergent changes in muscle metabolism depend on duration of high-altitude ancestry across Andean waterfowl
title_sort convergent changes in muscle metabolism depend on duration of high altitude ancestry across andean waterfowl
topic birds
high-altitude adaptation
hypoxia
energy metabolism
myoglobin
muscle energetics
url https://elifesciences.org/articles/56259
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AT luisalza convergentchangesinmusclemetabolismdependondurationofhighaltitudeancestryacrossandeanwaterfowl
AT gabrielenandal convergentchangesinmusclemetabolismdependondurationofhighaltitudeancestryacrossandeanwaterfowl
AT grahamrscott convergentchangesinmusclemetabolismdependondurationofhighaltitudeancestryacrossandeanwaterfowl
AT kevingmccracken convergentchangesinmusclemetabolismdependondurationofhighaltitudeancestryacrossandeanwaterfowl