Aging Cell (2003) 2, pp265–275 Doi: 10.1046/j.1474-9728.2003.00061.x © Blackwell Publishing Ltd/Anatomical Society of Great Britain and Ireland 2003 265 Blackwell Publishing Ltd. Age-related changes in the metabolism and body composition of three dog breeds and their relationship to life expectancy J. R. Speakman, 1,2 A. van Acker 3 and E. J. Harper 3 1 Aberdeen Centre for Energy Regulation and Obesity (ACERO), School of Biological Sciences, Zoology Building, University of Aberdeen, Aberdeen AB24 2TZ, UK 2 ACERO, Division of Energy Balance and Obesity, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK 3 Waltham Centre for Pet Nutrition, Waltham on the Wolds, Melton Mowbray, Leicestershire LE14 4SE, UK Summary We measured body composition and resting metabolic rates (RMR) of three dog breeds (Papillons, mean body mass 3.0 kg (n = 35), Labrador retrievers, mean body mass 29.8 kg (n = 35) and Great Danes, mean body mass 62.8 kg (n = 35)) that varied between 0.6 and 14.3 years of age. In Papillons, lean body mass (LBM) increased with age but fat mass (FBM) was constant; in Labradors, both LBM and FBM were constant with age, and in Great Danes, FBM increased with age but LBM was constant. FBM averaged 14.8% and 15.7% of body mass in Papillons and Labra- dors, respectively. Great Danes were leaner and averaged only 10.5% FBM. Pooling the data for all individuals, the RMR was significantly and positively associated with LBM and FBM and negatively associated with age. Once these factors had been taken into account there was still a significant breed effect on RMR, which was significantly lower in Labradors than in the other two breeds. Using the predictive multiple regression equation for RMR and the temporal trends in body composition, we modelled the expenditure of energy (at rest) over the first 8 years of life, and over the entire lifespan for each breed. Over the first 8 years of life the average expenditure of energy per kg LBM were 0.985, 0.675 and 0.662 GJ for Papillons, Labradors and Great Danes, respectively. This energy expenditure was almost 60% greater for the smallest compared with the largest breed. On average, however, the life expectancy for the smallest breed was a further 6 years (i.e. 14 years in total), whereas for the largest breed it was only another 6 months (i.e. 8.5 years in total). Total lifetime expenditure of energy at rest per kg LBM averaged 1.584, 0.918 and 0.691 GJ for Papillons, Labradors and Great Danes, respectively. In Labradors, total daily energy expenditure, measured by the doubly labelled water method in eight animals, was only 16% greater than the observed RMR. High energy expenditure in dogs appears positively linked to increased life expectancy, contrary to the finding across mammal species and within exotherms, yet resembling observations in other intra- specific studies. These contrasting correlations suggest that metabolism is affecting life expectancy in different ways at these different levels of enquiry. Key words: body composition; free-radical theory; metabolic rate; oxidative damage; rate of living. Introduction Among the oldest of the current theories of why we age is the ‘rate of living’ theory (Rubner, 1908; Pearl, 1928), which sug- gests that increases in metabolism of individuals shortens their lifespan. Comparisons of the metabolic rates and lifespans of different mammalian species provide support for this hypothe- sis. Rubner (1908) noted that the mass-specific rate of metab- olism decreases as mammals become larger, concomitant with an increase in their lifespans. More refined measures of mass- specific metabolic rate across a wide range of mammals (Brody, 1945; Kleiber, 1961) revealed that the interspecific scaling expo- nent for metabolic rate was around -0.27, whereas the scaling of lifespan in mammals was around +0.29 (Sacher, 1977). The product of the two traits, expressing the lifespan expenditure of energy per gram of tissue, is consequently virtually independ- ent of mass across a broad spectrum of mammals (Calder, 1984), a so-called life history invariant (Charnov, 1993). The ‘rate of living’ theory was further strengthened when Harman (1956) proposed a mechanism whereby oxygen consumption might be linked to aging and lifespan. Harman (1956) suggested that free-radicals, produced as a by-product of oxidative phos- phorylation, damage macromolecules, leading to physiological attrition (aging) and ultimate failure (death). Conceptually the ‘metabolism – free-radical – aging’ hypothesis is extremely appealing (Arking, 1998; Beckman & Ames, 1998; Sohal, 2002; Sohal et al., 2002) and amenable to experimental testing (Golden et al., 2002), although it is not universally accepted (see debate in Jacobs, 2003a,b; Pak et al., 2003a,b). More recently, however, the growing consensus around the idea has started to collapse. It was noted that there are many exceptions to the fixed ‘amount of living’ estimates derived Correspondence J. R. Speakman, Aberdeen Centre for Energy regulation and Obesity (ACERO), School of Biological Sciences, Zoology Building, Tillydrone Ave., University of Aberdeen, Aberdeen AB24 2TZ, Scotland, UK. E-mail: j.speakman@abdn.ac.uk Accepted for publication 12 August 2003