Diet fatty acid profile, membrane composition and lifespan: An experimental study using the blowfly (Calliphora stygia)

Highlights

• Membrane fatty acid composition may be an important determinant of maximum lifespan.

• We report on three experiments manipulating dietary fatty acids in blowflies.

• Peroxidation index was relatively refractory to changes in diet.

• Changing dietary fatty acids had little effect on maximum lifespan.

Abstract

The membrane pacemaker theory of ageing proposes that the polyunsaturated fatty acid (PUFA) composition of membrane lipids of a species is an important determinant of its maximum lifespan. We report three experiments using the blowfly Calliphora stygia, where this theory was tested by manipulation of dietary fat profile. Although the fat profile of the larval diet resulted in small alterations of individual membrane fatty acids, it had no effect on the peroxidation index (PI) of membrane lipids and furthermore had no effect on maximum lifespan. Similarly, manipulation of the fat profile of the adult diet resulted in small changes in individual fatty acids, but had no effect on the PI of membrane lipids. There was a small increase in maximum lifespan when adult diet was supplemented with PUFA in form of vegetable oils but no effect when diet was supplemented with pure PUFA. This difference is possibly due to antioxidant content of vegetable oils. The relative refractoriness of membrane PI to dramatic changes in response to diet is similar to the situation in the rat. These results also indicate the blowfly is unable to convert 18-carbon PUFA to more highly polyunsaturated 20- and 22-carbon PUFA.

Introduction

Animal species have distinctive maximum lifespans and there are several theories about the mechanisms of ageing that might determine lifespan, but no universal agreement about these processes. One theory, the ‘membrane pacemaker’ theory, is a modification of the oxidative stress theory of ageing and proposes that the fatty acid composition of membranes (especially mitochondrial membranes) may be an important component determining maximum lifespan and ageing of animals (Pamplona et al., 1998, Hulbert, 2005). This theory is based on the fact that fatty acids differ dramatically in their susceptibility to peroxidation (Holman, 1954). Fatty acids include saturated fatty acids (SFA), monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA), but only PUFA undergo significant lipid peroxidation, with the more polyunsaturated the PUFA the more prone it is to peroxidative damage. By contrast, the SFA and MUFA are highly resistant to peroxidative damage. The membrane pacemaker theory proposes that the link between membrane composition and lifespan determination is that the peroxidative susceptibility of membranes determines the degree of lipid peroxidation and the consequent damage to other important biomolecules from the products of PUFA peroxidation (see Hulbert et al., 2007).

The development of the ‘membrane pacemaker’ theory of ageing originated largely from correlations between membrane fatty acid composition and maximum lifespan of mammal and bird species (for review see Hulbert et al., 2007). More recent studies also provide evidence of correlations between membrane composition and longevity in some invertebrate species, including honeybees (Haddad et al., 2007), bivalve molluscs (Munro and Blier, 2012) and the nematode Caenorhabditis elegans (Shmookler Reis et al., 2011). Most evidence to date is correlational and therefore requires manipulation of membrane fatty acid composition to determine if the relationship is one of cause and effect. An obvious experimental test of the ‘membrane pacemaker’ theory would be to alter membrane fatty acid composition by diet manipulation, and determine whether such membrane changes also alter animal longevity in a predicted manner.

Because of both their relatively short adult lifespans and low husbandry costs, some invertebrate species (e.g. Drosophila and C. elegans) have been used to experimentally test theories of ageing. We have previously examined ageing in the blowfly, Calliphora stygia and suggested it is a good model organism to study mechanisms of ageing as it has both a short adult lifespan and the additional advantage of being large enough (body mass ∼70 mg) to measure the biochemistry and physiology of individuals (Hulbert et al., 2004, Ujvari et al., 2009, Kelly et al., 2013). In blowflies, the larval life stage is the one with the greatest growth and thus involves considerable membrane formation while the adult life stage involves negligible growth (and thus negligible new membrane formation) and changes in membrane composition will likely only be the result of membrane lipid turnover. We have experimentally investigated both life stages and report the findings of three separate experiments designed to test the ‘membrane pacemaker’ theory of ageing. Testing whether manipulation of dietary fatty acid composition changes membrane fatty acid composition and consequently also changes adult lifespan of this blowfly. The first experiment changed membrane fatty acid composition of blowfly larvae (by manipulation of the larval diet) and determined whether lifespan of the adult blowfly was affected. The other two experiments manipulated fatty acid composition the adult diet of the blowfly and whether these treatments affected adult lifespan of the blowfly.