Evidence Against the Membrane Pacemaker Hypothesis of Aging in Bird Species

The membrane pacemaker hypothesis suggests that the lipid composition of membranes, and particularly mitochondrial membranes, is an important determinant of species longevity in at least some clades, such as mammals and birds. Membrane composition determines the degree of resistance to lipid oxidation and consequent loss of function for component parts of a cell. Aging is associated with a rise in oxidative stress placed upon cells and their structures, related to chronic inflammation and mitochondrial dysfunction.

Over the years, a fair amount of supporting evidence has been gathered for this view of species longevity, but the paper here stands in opposition to that work, at least for bird species. It is worth noting that birds, and other flying species, are metabolically quite different from near relative non-flying species. The high metabolic demands of flight lead to adaptations that clearly impact aging in many cases, such as for some bat species with noted longevity, perhaps largely through mitochondrial function, perhaps not. That said, the membrane pacemaker hypothesis was thought to be relevant in both mammals and birds. As usual, all too little is simple, straightforward, and a settled matter when it comes to the details of cellular metabolism and aging.

No Evidence for Trade-Offs Between Lifespan, Fecundity, and Basal Metabolic Rate Mediated by Liver Fatty Acid Composition in Birds

The fatty acid composition of biological membranes has been hypothesised to be a key molecular adaptation associated with the evolution of metabolic rates, ageing, and life span - the basis of the membrane pacemaker hypothesis (MPH). MPH proposes that highly unsaturated membranes enhance cellular metabolic processes while being more prone to oxidative damage, thereby increasing the rates of metabolism and ageing. MPH could, therefore, provide a mechanistic explanation for trade-offs between longevity, fecundity, and metabolic rates, predicting that short-lived species with fast metabolic rates and higher fecundity would have greater levels of membrane unsaturation.

However, previous comparative studies testing MPH provide mixed evidence regarding the direction of covariation between fatty acid unsaturation and life span or metabolic rate. Moreover, some empirical studies suggest that an n-3/n-6 PUFA ratio or the fatty acid chain length, rather than the overall unsaturation, could be the key traits coevolving with life span. In this study, we tested the coevolution of liver fatty acid composition with maximum life span, annual fecundity, and basal metabolic rate (BMR), using a recently published data set comprising liver fatty acid composition of 106 avian species.

While statistically controlling for the confounding effects of body mass and phylogeny, we found no support for long life span evolving with low fatty acid unsaturation and only very weak support for fatty acid unsaturation acting as a pacemaker of BMR. Moreover, our analysis provided no evidence for the previously reported links between life span and n-3 PUFA/total PUFA or MUFA proportion.

Our results rather suggest that long life span evolves with long-chain fatty acids irrespective of their degree of unsaturation as life span was positively associated with at least one long-chain fatty acid of each type (i.e., SFA, MUFA, n-6 PUFA, and n-3 PUFA). Importantly, maximum life span, annual fecundity, and BMR were associated with different fatty acids or fatty acid indices, indicating that longevity, fecundity, and BMR coevolve with different aspects of fatty acid composition. Therefore, in addition to posing significant challenges to MPH, our results imply that fatty acid composition does not pose an evolutionary constraint underpinning life-history trade-offs at the molecular level.

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