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

Sampath A Kumar,Oldřich Tomášek,Ondřej Kauzál,Tomáš Albrecht

doi:10.3389/fcell.2021.638501

Abstract

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.

Highlights

The fatty acid (FA) composition of biological membranes has a strong influence on many cellular processes (Grecco et al, 2011)
Index of overall FA unsaturation (DBI) and peroxidizability index (PI) were strongly positively correlated to average chain length (ACL) and polyunsaturated FA (PUFA) (Figure 2)
Our comparative analysis does not support the membrane pacemaker hypothesis (MPH) as a whole because none of the key indices of FA unsaturation (DBI, PI, saturated FA (SFA), monounsaturated FA (MUFA), and PUFA) covaried with maximum life span, basal metabolic rate (BMR), or annual fecundity when controlled for the confounding effects of body mass, migration behaviour and phylogeny

Summary

Introduction

The fatty acid (FA) composition of biological membranes has a strong influence on many cellular processes (Grecco et al, 2011) This fact has sparked the development of hypotheses that propose that the membrane FA composition is a key molecular adaptation underpinning the evolution of metabolic rates, ageing, and life span (Hulbert and Else, 1999; Pamplona et al, 2002; Hulbert, 2010). The addition of polyunsaturated FA (PUFA) modifies the spatial distribution of lipid rafts (i.e., the relatively ordered and rigid membrane lipid regions), pushing them closer to each other and stabilising raft-associated proteins (Shaikh et al, 2015) Both membrane fluidity and the effect of PUFA on the spatial distribution of lipid rafts may enhance the activity of membrane proteins important for energetic metabolism, such as glucose transporter proteins (Weijers, 2016) and Na+/K+ ATPases (Lingwood et al, 2005; Welker et al, 2007), respectively. In addition to enhanced metabolic rates, higher membrane unsaturation can increase the rate of senescence according to MPH because the accumulation of oxidative damage has been proposed as a major cause of senescence by the free-radical theory of ageing (Barja, 2013)

Methods

Results

Conclusion