Lifespan and reproduction in Drosophila: New insights from nutritional geometry

Modest dietary restriction (DR) prolongs life in a wide range of organisms, spanning single-celled yeast to mammals. Here, we report the use of recent techniques in nutrition research to quantify the detailed relationship between diet, nutrient intake, lifespan, and reproduction in Drosophila melanogaster. Caloric restriction (CR) was not responsible for extending lifespan in our experimental flies. Response surfaces for lifespan and fecundity were maximized at different protein–carbohydrate intakes, with longevity highest at a protein-to-carbohydrate ratio of 1:16 and egg-laying rate maximized at 1:2. Lifetime egg production, the measure closest to fitness, was maximized at an intermediate P:C ratio of 1:4. Flies offered a choice of complementary foods regulated intake to maximize lifetime egg production. The results indicate a role for both direct costs of reproduction and other deleterious consequences of ingesting high levels of protein. We unite a body of apparently conflicting work within a common framework and provide a platform for studying aging in all organisms.

[1]  S. Benzer,et al.  Compensatory ingestion upon dietary restriction in Drosophila melanogaster , 2005, Nature Methods.

[2]  S. Simpson,et al.  Caloric restriction and aging revisited: the need for a geometric analysis of the nutritional bases of aging. , 2007, The journals of gerontology. Series A, Biological sciences and medical sciences.

[3]  L. Guarente,et al.  Calorie restriction, SIRT1 and metabolism: understanding longevity , 2005, Nature Reviews Molecular Cell Biology.

[4]  R. Sibly,et al.  Optimal foraging when regulating intake of multiple nutrients , 2004, Animal Behaviour.

[5]  G. Barja,et al.  Protein Restriction Without Strong Caloric Restriction Decreases Mitochondrial Oxygen Radical Production and Oxidative DNA Damage in Rat Liver , 2004, Journal of bioenergetics and biomembranes.

[6]  S. Simpson,et al.  Integrative models of nutrient balancing: application to insects and vertebrates , 1997, Nutrition Research Reviews.

[7]  Luc F. Bussière,et al.  High-quality male field crickets invest heavily in sexual display but die young , 2004, Nature.

[8]  L. Partridge,et al.  Special issue on dietary restriction: Dietary restriction, longevity and ageing—the current state of our knowledge and ignorance , 2005, Mechanisms of Ageing and Development.

[9]  L. Partridge,et al.  No extension of lifespan by ablation of germ line in Drosophila , 2006, Proceedings of the Royal Society B: Biological Sciences.

[10]  Richard Weindruch,et al.  The Retardation of Aging and Disease by Dietary Restriction , 1988 .

[11]  H. Aguilaniu,et al.  PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans , 2007, Nature.

[12]  L. Partridge,et al.  Counting the calories: the role of specific nutrients in extension of life span by food restriction. , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[13]  S. Nemoto,et al.  Ageing and the mystery at Arles , 2004, Nature.

[14]  M. Blows,et al.  Measuring Nonlinear Selection , 2003, The American Naturalist.

[15]  J. A. Zimmerman,et al.  Nutritional control of aging , 2003, Experimental Gerontology.

[16]  S. Chenoweth,et al.  Contrasting Mutual Sexual Selection on Homologous Signal Traits in Drosophila serrata , 2004, The American Naturalist.

[17]  L. Partridge,et al.  Sex and Death: What Is the Connection? , 2005, Cell.

[18]  L. Partridge,et al.  Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  L. Guarente,et al.  Genetic pathways that regulate ageing in model organisms , 2000, Nature.

[20]  S. Benzer,et al.  Regulation of Lifespan in Drosophila by Modulation of Genes in the TOR Signaling Pathway , 2004, Current Biology.

[21]  L. Partridge,et al.  Dietary Restriction in Drosophila: Delayed Aging or Experimental Artefact? , 2007, PLoS genetics.

[22]  M. Tatar,et al.  Restriction of amino acids extends lifespan in Drosophila melanogaster , 2006, Mechanisms of Ageing and Development.

[23]  Edward J Masoro,et al.  Caloric restriction and aging: controversial issues. , 2006, The journals of gerontology. Series A, Biological sciences and medical sciences.

[24]  B. Merry.  Molecular mechanisms linking calorie restriction and longevity. , 2002, The international journal of biochemistry & cell biology.

[25]  E. Ravussin,et al.  Calorie restriction and aging: review of the literature and implications for studies in humans. , 2003, The American journal of clinical nutrition.

[26]  S. Simpson,et al.  Does Bertrand's rule apply to macronutrients? , 2005, Proceedings of the Royal Society B: Biological Sciences.

[27]  M. Tatar,et al.  Drosophila diet restriction in practice: Do flies consume fewer nutrients? , 2006, Mechanisms of Ageing and Development.

[28]  Kyung-Jin Min,et al.  Counting calories in Drosophila diet restriction , 2007, Experimental Gerontology.

[29]  S. Benzer,et al.  Prandiology of Drosophila and the CAFE assay , 2007, Proceedings of the National Academy of Sciences.

[30]  L. Partridge,et al.  Calories Do Not Explain Extension of Life Span by Dietary Restriction in Drosophila , 2005, PLoS biology.