Mitochondrial uncoupling as a regulator of life-history trajectories in birds

an experimental study in the zebra finch

Antoine Stier*, Pierre Bize, Damien Roussel, Quentin Schull, Sylvie Massemin, Francois Criscuolo

*Corresponding author for this work

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Mitochondria have a fundamental role in the transduction of energy from food into ATP. The coupling between food oxidation and ATP production is never perfect, but may nevertheless be of evolutionary significance. The 'uncoupling to survive' hypothesis suggests that 'mild' mitochondrial uncoupling evolved as a protective mechanism against the excessive production of damaging reactive oxygen species (ROS). Because resource allocation and ROS production are thought to shape animal life histories, alternative life-history trajectories might be driven by individual variation in the degree of mitochondrial uncoupling. We tested this hypothesis in a small bird species, the zebra finch (Taeniopygia guttata), by treating adults with the artificial mitochondrial uncoupler 2,4-dinitrophenol (DNP) over a 32-month period. In agreement with our expectations, the uncoupling treatment increased metabolic rate. However, we found no evidence that treated birds enjoyed lower oxidative stress levels or greater survival rates, in contrast to previous results in other taxa. In vitro experiments revealed lower sensitivity of ROS production to DNP in mitochondria isolated from skeletal muscles of zebra finch than mouse. In addition, we found significant reductions in the number of eggs laid and in the inflammatory immune response in treated birds. Altogether, our data suggest that the 'uncoupling to survive' hypothesis may not be applicable for zebra finches, presumably because of lower effects of mitochondrial uncoupling on mitochondrial ROS production in birds than in mammals. Nevertheless, mitochondrial uncoupling appeared to be a potential life-history regulator of traits such as fecundity and immunity at adulthood, even with food supplied ad libitum.

Original languageEnglish
Pages (from-to)3579-3589
Number of pages11
JournalJournal of Experimental Biology
Volume217
Issue number19
Early online date1 Oct 2014
DOIs
Publication statusPublished - 1 Oct 2014

Keywords

  • Mitochondria
  • Uncoupling
  • Free radical theory of ageing
  • Oxidative stress
  • Reactive oxygen species
  • Life-history trade-off
  • Bird

Cite this

Mitochondrial uncoupling as a regulator of life-history trajectories in birds : an experimental study in the zebra finch. / Stier, Antoine; Bize, Pierre; Roussel, Damien; Schull, Quentin; Massemin, Sylvie; Criscuolo, Francois.

In: Journal of Experimental Biology, Vol. 217, No. 19, 01.10.2014, p. 3579-3589.

Research output: Contribution to journalArticle

Stier, Antoine ; Bize, Pierre ; Roussel, Damien ; Schull, Quentin ; Massemin, Sylvie ; Criscuolo, Francois. / Mitochondrial uncoupling as a regulator of life-history trajectories in birds : an experimental study in the zebra finch. In: Journal of Experimental Biology. 2014 ; Vol. 217, No. 19. pp. 3579-3589.
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abstract = "Mitochondria have a fundamental role in the transduction of energy from food into ATP. The coupling between food oxidation and ATP production is never perfect, but may nevertheless be of evolutionary significance. The 'uncoupling to survive' hypothesis suggests that 'mild' mitochondrial uncoupling evolved as a protective mechanism against the excessive production of damaging reactive oxygen species (ROS). Because resource allocation and ROS production are thought to shape animal life histories, alternative life-history trajectories might be driven by individual variation in the degree of mitochondrial uncoupling. We tested this hypothesis in a small bird species, the zebra finch (Taeniopygia guttata), by treating adults with the artificial mitochondrial uncoupler 2,4-dinitrophenol (DNP) over a 32-month period. In agreement with our expectations, the uncoupling treatment increased metabolic rate. However, we found no evidence that treated birds enjoyed lower oxidative stress levels or greater survival rates, in contrast to previous results in other taxa. In vitro experiments revealed lower sensitivity of ROS production to DNP in mitochondria isolated from skeletal muscles of zebra finch than mouse. In addition, we found significant reductions in the number of eggs laid and in the inflammatory immune response in treated birds. Altogether, our data suggest that the 'uncoupling to survive' hypothesis may not be applicable for zebra finches, presumably because of lower effects of mitochondrial uncoupling on mitochondrial ROS production in birds than in mammals. Nevertheless, mitochondrial uncoupling appeared to be a potential life-history regulator of traits such as fecundity and immunity at adulthood, even with food supplied ad libitum.",
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