|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online April 26, 2005
Journal of Experimental Biology 208, 1717-1730 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01556
Review article: Lifespan, reproduction and ecology |
Body size, energy metabolism and lifespan
Aberdeen Centre for Energy regulation and Obesity (ACERO), School of Biological Sciences, University of Aberdeen, Aberdeen AB24 2TZ, Scotland, UK and ACERO, Division of Energy Balance and Obesity, Rowett Research Institute, Bucksburn, Aberdeen, AB21 9SB, Scotland, UK
e-mail: J.Speakman{at}abdn.ac.uk
Accepted 23 February 2005
Summary
Bigger animals live longer. The scaling exponent for the relationship between lifespan and body mass is between 0.15 and 0.3. Bigger animals also expend more energy, and the scaling exponent for the relationship of resting metabolic rate (RMR) to body mass lies somewhere between 0.66 and 0.8. Mass-specific RMR therefore scales with a corresponding exponent between -0.2 and -0.33. Because the exponents for mass-specific RMR are close to the exponents for lifespan, but have opposite signs, their product (the mass-specific expenditure of energy per lifespan) is independent of body mass (exponent between -0.08 and 0.08). This means that across species a gram of tissue on average expends about the same amount of energy before it dies regardless of whether that tissue is located in a shrew, a cow, an elephant or a whale. This fact led to the notion that ageing and lifespan are processes regulated by energy metabolism rates and that elevating metabolism will be associated with premature mortality - the rate of living theory.
The free-radical theory of ageing provides a potential mechanism that links metabolism to ageing phenomena, since oxygen free radicals are formed as a by-product of oxidative phosphorylation. Despite this potential synergy in these theoretical approaches, the free-radical theory has grown in stature while the rate of living theory has fallen into disrepute. This is primarily because comparisons made across classes (for example, between birds and mammals) do not conform to the expectations, and even within classes there is substantial interspecific variability in the mass-specific expenditure of energy per lifespan. Using interspecific data to test the rate of living hypothesis is, however, confused by several major problems. For example, appeals that the resultant lifetime expenditure of energy per gram of tissue is `too variable' depend on the biological significance rather than the statistical significance of the variation observed. Moreover, maximum lifespan is not a good marker of ageing and RMR is not a good measure of total energy metabolism. Analysis of residual lifespan against residual RMR reveals no significant relationship. However, this is still based on RMR.
A novel comparison using daily energy expenditure (DEE), rather than BMR, suggests that lifetime expenditure of energy per gram of tissue is NOT independent of body mass, and that tissue in smaller animals expends more energy before expiring than tissue in larger animals. Some of the residual variation in this relationship in mammals is explained by ambient temperature. In addition there is a significant negative relationship between residual lifespan and residual daily energy expenditure in mammals. A potentially much better model to explore the links of body size, metabolism and ageing is to examine the intraspecific links. These studies have generated some data that support the original rate of living theory and other data that conflict. In particular several studies have shown that manipulating animals to expend more or less energy generate the expected effects on lifespan (particularly when the subjects are ectotherms). However, smaller individuals with higher rates of metabolism live longer than their slower, larger conspecifics.
An addition to these confused observations has been the recent suggestion that under some circumstances we might expect mitochondria to produce fewer free radicals when metabolism is higher - particularly when they are uncoupled. These new ideas concerning the manner in which mitochondria generate free radicals as a function of metabolism shed some light on the complexity of observations linking body size, metabolism and lifespan.
Key words: ageing, rate of living theory, free radical, oxidative stress
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  J. Lapointe, Z. Stepanyan, E. Bigras, and S. Hekimi Reversal of the Mitochondrial Phenotype and Slow Development of Oxidative Biomarkers of Aging in Long-lived Mclk1+/- Mice J. Biol. Chem., July 24, 2009; 284(30): 20364 - 20374. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. I. Tieleman, M. A Versteegh, A. Fries, B. Helm, N. J Dingemanse, H. L. Gibbs, and J. B Williams Genetic modulation of energy metabolism in birds through mitochondrial function Proc R Soc B, May 7, 2009; 276(1662): 1685 - 1693. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Moe, B. Ronning, S. Verhulst, and C. Bech Metabolic ageing in individual zebra finches Biol Lett, February 23, 2009; 5(1): 86 - 89. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. G. Valencak, F. Tataruch, and T. Ruf Peak energy turnover in lactating European hares: the role of fat reserves J. Exp. Biol., January 15, 2009; 212(2): 231 - 237. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Lapointe and S. Hekimi Early Mitochondrial Dysfunction in Long-lived Mclk1+/- Mice J. Biol. Chem., September 19, 2008; 283(38): 26217 - 26227. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Selman, J. S McLaren, A. R Collins, G. G Duthie, and J. R Speakman The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis Proc R Soc B, August 22, 2008; 275(1645): 1907 - 1916. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Ruggiero, E. J. Metter, V. Melenovsky, A. Cherubini, S. S. Najjar, A. Ble, U. Senin, D. L. Longo, and L. Ferrucci High Basal Metabolic Rate Is a Risk Factor for Mortality: The Baltimore Longitudinal Study of Aging J Gerontol A Biol Sci Med Sci, July 1, 2008; 63(7): 698 - 706. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Delanaye, E. Cavalier, and J.-M. Krzesinski Cystatin C, Renal Function, and Cardiovascular Risk Ann Intern Med, February 19, 2008; 148(4): 323 - 323. [Full Text] [PDF]
|
|
|
|
 |
|
 P. Wiersma, M. A. Chappell, and J. B. Williams Cold- and exercise-induced peak metabolic rates in tropical birds PNAS, December 26, 2007; 104(52): 20866 - 20871. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J. Hulbert, R. Pamplona, R. Buffenstein, and W. A. Buttemer Life and Death: Metabolic Rate, Membrane Composition, and Life Span of Animals Physiol Rev, October 1, 2007; 87(4): 1175 - 1213. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Moe, F. Angelier, C. Bech, and O. Chastel Is basal metabolic rate influenced by age in a long-lived seabird, the snow petrel? J. Exp. Biol., October 1, 2007; 210(19): 3407 - 3414. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Lanfear, J. A. Thomas, J. J. Welch, T. Brey, and L. Bromham Metabolic rate does not calibrate the molecular clock PNAS, September 25, 2007; 104(39): 15388 - 15393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Rottenberg Exceptional longevity in songbirds is associated with high rates of evolution of cytochrome b, suggesting selection for reduced generation of free radicals J. Exp. Biol., June 15, 2007; 210(12): 2170 - 2180. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. d. Magalhaes, J. Costa, and G. M. Church An Analysis of the Relationship Between Metabolism, Developmental Schedules, and Longevity Using Phylogenetic Independent Contrasts J Gerontol A Biol Sci Med Sci, February 1, 2007; 62(2): 149 - 160. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Wang, K. Seburn, L. Bechtel, B. Y. Lee, J. P. Szatkiewicz, P. M. Nishina, and J. K. Naggert Defective carbohydrate metabolism in mice homozygous for the tubby mutation Physiol Genomics, October 11, 2006; 27(2): 131 - 140. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Ruggiero and L. Ferrucci The Endeavor of High Maintenance Homeostasis: Resting Metabolic Rate and the Legacy of Longevity J Gerontol A Biol Sci Med Sci, May 1, 2006; 61(5): 466 - 473. [Abstract] [Full Text] [PDF]
|
|
