The Long Life of Birds: The Rat-Pigeon Comparison Revisited

Abstract

The most studied comparison of aging and maximum lifespan potential (MLSP) among endotherms involves the 7-fold longevity difference between rats (MLSP 5y) and pigeons (MLSP 35y). A widely accepted theory explaining MLSP differences between species is the oxidative stress theory, which purports that reactive oxygen species (ROS) produced during mitochondrial respiration damage bio-molecules and eventually lead to the breakdown of regulatory systems and consequent death. Previous rat-pigeon studies compared only aspects of the oxidative stress theory and most concluded that the lower mitochondrial superoxide production of pigeons compared to rats was responsible for their much greater longevity. This conclusion is based mainly on data from one tissue (the heart) using one mitochondrial substrate (succinate). Studies on heart mitochondria using pyruvate as a mitochondrial substrate gave contradictory results. We believe the conclusion that birds produce less mitochondrial superoxide than mammals is unwarranted.We have revisited the rat-pigeon comparison in the most comprehensive manner to date. We have measured superoxide production (by heart, skeletal muscle and liver mitochondria), five different antioxidants in plasma, three tissues and mitochondria, membrane fatty acid composition (in seven tissues and three mitochondria), and biomarkers of oxidative damage. The only substantial and consistent difference that we have observed between rats and pigeons is their membrane fatty acid composition, with rats having membranes that are more susceptible to damage. This suggests that, although there was no difference in superoxide production, there is likely a much greater production of lipid-based ROS in the rat.We conclude that the differences in superoxide production reported previously were due to the arbitrary selection of heart muscle to source mitochondria and the provision of succinate. Had mitochondria been harvested from other tissues or other relevant mitochondrial metabolic substrates been used, then very different conclusions regarding differences in oxidative stress would have been reached.

Mitochondrial uncoupling as a regulator of life history trajectories in birds: An experimental study in the zebra finch

“…5D) ROS production of the zebra finch compared with the mouse might appear contradictory to the initial idea that avian mitochondria produce fewer ROS than mammalian mitochondria. However, this idea has recently been seriously questioned (Montgomery et al, 2011), and our results are in accordance with the results of two recent studies comparing birds and mammals (Montgomery et al, 2011;Kuzmiak et al, 2012).…”

“…Finally, avian mitochondria could be less sensitive than other taxa to mitochondrial uncoupling in terms of ROS production (present study; P.B., unpublished results in Japanese quail). Avian mitochondria are known to differ from mammalian ones in some characteristics, such as ROS production (Ku and Sohal, 1993;Lambert et al, 2010; but see Montgomery et al, 2011) and mitochondrial membrane fatty acid composition (Pamplona et al, 1999;Montgomery et al, 2011). According to this idea, our in vitro results suggest that the ROS production of zebra finch mitochondria is less sensitive to mitochondrial uncoupling than the ROS production of mouse mitochondria, at least when the respiration is fuelled with pyruvate-malate (Fig.…”

Linkages between the life-history evolution of tropical and temperate birds and the resistance of their cells to oxidative and non-oxidative chemical injury

“…Also, lipid peroxidation products are known to damage nearby macromolecules including proteins, a process that has consequences for aging (Pamplona et al, 1999). These ideas suggest that tropical birds have a low degree of fatty acid unsaturation in their membranes, which might protect them from oxidative damage (Pamplona et al, 1999;Montgomery et al, 2011). In summary, we found that primary cell lines derived from tropical birds are more resistant to some cellular stressors compared with cells from their temperate counterparts.…”

Loss of integration is associated with reduced resistance to oxidative stress

“…A previously published method (Levine et al, 1990) (see also Cao and Cutler, 1995;Montgomery et al, 2011) was used to quantify the concentration of protein carbonyls in plasma. Protein carbonyls indicate protein oxidative damage.…”