Nutritional ecology and the evolution of aging

Experimental Gerontology

Volumn 86, Issue , 2016, Pages 50-61

  Raubenheimer, David ^a   Simpson, Stephen J ^a   Le Couteur, David G ^a,b   Solon Biet, Samantha M ^a,b   Coogan, Sean C P ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ANZAC Research Institute   (Australia)

Author keywords

Aging; Evolution; Geometric Framework; Healthspan; Lifespan; Longevity

Indexed keywords

AGING; AMINO ACID COMPOSITION; ANIMAL BEHAVIOR; ARTICLE; CALORIC RESTRICTION; DIET RESTRICTION; DIETARY INTAKE; ENVIRONMENTAL FACTOR; EVOLUTION; FEEDING BEHAVIOR; FITNESS; FOOD COMPOSITION; HOMEOSTASIS; LIFESPAN; MACRONUTRIENT; NATURAL SELECTION; NONHUMAN; NUTRIENT CONTENT; PRIORITY JOURNAL; REPRODUCTION; ANIMAL; CARBOHYDRATE DIET; DIET; FOOD; LONGEVITY; PHARMACOLOGY; PHYSIOLOGY; PROCEDURES; PROTEIN INTAKE;

CARBOHYDRATE DIET; PROTEIN INTAKE;

AGING; ANIMALS; CALORIC RESTRICTION; DIET; DIETARY CARBOHYDRATES; DIETARY PROTEINS; FOOD; HOMEOSTASIS; LONGEVITY; REPRODUCTION;

EID: 84969174923     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2016.04.007     Document Type: Article

References (83)

1. Adler, M.I., Bonduriansky, R., Why do the well-fed appear to die young?. BioEssays 36 (2014), 439–450.
2. Adler, M.I., Bonduriansky, R., Sexual conflict, life span, and ageing. Cold Spring Harb. Perspect. Biol., 2015, 10.1101/cshperspect.a017566.
3. Archer, C.R., Hunt, J., Understanding the link between sexual selection, sexual conflict and aging using crickets as a model. Exp. Gerontol. 71 (2015), 4–13.
4. Bilinski, T., Paszkiewicz, T., Zadrag-Tecza, R., Energy excess is the main cause of accelerated aging of mammals. Oncotarget 6 (2015), 12909–12919.
5. Bilsborough, S., Mann, N., A review of issues of dietary protein intake in humans. Int. J. Sport Nutr. Excerc. Metab. 16 (2006), 129–152.
6. Brent, L.J.N., Franks, D.W., Foster, E.A., Balcomb, K.C., Cant, M.A., Croft, D.P., Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr. Biol. 25 (2015), 746–750.
7. Calow, P., Towards a definition of functional ecology. Funct. Ecol. 1 (1987), 57–61.
8. Cesari, M., Vellas, B., Gambassi, G., The stress of aging. Exp. Gerontol. 48 (2013), 451–456.
9. Chambers, P.G., Simpson, S.J., Raubenheimer, D., Behavioural mechanisms of nutrient balancing in Locusta migratoria. Anim. Behav. 50 (1995), 1513–1523.
10. Cheplick, G.P., Plant Evolutionary Ecology. 2015, Oxford University Press, Oxford, New York.
11. Dev, S.B., Unsolved problems in biology—the state of current thinking. Prog. Biophys. Mol. Biol. 117 (2015), 232–239.
12. Eisert, R., Hypercarnivory and the brain: protein requirements of cats reconsidered. J. Comp. Physiol. B. 181 (2011), 1–17.
13. Fanson, B.G., Taylor, P.W., Protein:carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast:sugar ratios. Age (Dordr.) 34 (2012), 1361–1368.
14. Fanson, B.G., Weldon, C.W., Perez-Staples, D., Simpson, S.J., Taylor, P.W., Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell 8 (2009), 514–523.
15. Felton, A.M., Felton, A., Wood, J.T., Foley, W.J., Raubenheimer, D., Wallis, I.R., Lindenmayer, D.B., Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. Int. J. Primatol. 30 (2009), 675–696.
16. Felton, A.M., Felton, A., Raubenheimer, D., Simpson, S.J., Foley, W.J., Wood, J.T., Wallis, I.R., Lindenmayer, D.B., Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav. Ecol. 20 (2009), 685–690.
17. Flatt, T., Heyland, A., Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-Offs. 2011, Oxford University Press.
18. Flatt, T., Schmidt, P.S., Integrating evolutionary and molecular genetics of aging. Biochim. Biophys. Acta Gen. Subj. 1790 (2009), 951–962.
19. Fletcher, Q.E., Selman, C., Aging in the wild: insights from free-living and non-model organisms. Exp. Gerontol. 71 (2015), 1–3.
20. Fontana, L., Partridge, L., Promoting health and longevity through diet: from model organisms to humans. Cell 161 (2015), 106–118.
21. Foster, M.S., Ecological and nutritional effects of food scarcity on a tropical frugivorous bird and its fruit source. Ecology 58 (1977), 73–85.
22. Evolutionary Ecology. Fox, C.W., Roff, D.A., Fairbairn, D.J., (eds.) Concepts and Case Studies, 2001, Oxford University Press, Oxford, New York.
23. Fredriksson, G.M., Wich, S.A., Trisno, Frugivory in sun bears (Helarctos malayanus) is linked to el Nino related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biol. J. Linn. Soc. 89 (2006), 489–508.
24. Gibbs, V.K., Smith, D.L., Nutrition and energetics in rodent longevity research. Experimental Gerontology, 2016, 10.1016/j.exger.2016.04.004.
25. Gosby, A.K., Conigrave, A.D., Raubenheimer, D., Simpson, S.J., Protein leverage and energy intake. Obes. Rev. 15 (2013), 183–191.
26. Harrison, S.J., Raubenheimer, D., Simpson, S.J., Godin, J.G., Bertram, S.M., Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein, carbohydrate and phosphorus on field cricket fitness. Proc. Biol. Sci., 281, 2014, 1792.
27. Hayflick, L., Biological Aging Is no longer an Unsolved Problem. Rattan, S.I.S., Akman, S., (eds.) Biogerontology: Mechanisms and Interventions, 2007, 1–13.
28. Hayflick, L., Entropy explains aging, genetic determinism explains longevity, and undefined terminology explains misunderstanding both. PLoS Genet. 3 (2007), 2351–2354.
29. Hughes, K.A., Reynolds, R.M., Evolutionary and mechanistic theories of aging. Annu. Rev. Entomol. 50 (2005), 421–445.
30. Irwin, M.T., Raharison, J.-L., Raubenheimer, D., Chapman, C.A., Rothman, J.M., The nutritional geometry of resource scarcity: effects of lean seasons and habitat disturbance on nutrient intakes and balancing in wild sifakas. PLoS One, 10, 2015, e0128046.
31. Jensen, K., Mayntz, D., Toft, S., Clissold, F.J., Hunt, J., Raubenheimer, D., Simpson, S.J., Optimal foraging for specific nutrients in predatory beetles. Proc. R. Soc. B 279 (2012), 2212–2218.
32. Jensen, K., McClure, C., Priest, N.K., Hunt, J., Sex-specific effects of protein and carbohydrate intake on reproduction but not lifespan in Drosophila melanogaster. Aging Cell 14 (2015), 605–615.
33. Johnson, C.A., Raubenheimer, D., Rothman, J.M., 30 days in the life: daily nutrient balancing in a wild chacma baboon. PLoS One, 8, 2013, e70383.
34. Kirkwood, T.B.L., Evolution of aging. Nature 270 (1977), 301–304.
35. Kohl, K.D., Coogan, S.C.P., Raubenheimer, D., Do wild carnivores forage for prey or nutrients? Evidence for nutrient-specific foraging in vertebrate predators. BioEssays 37 (2015), 701–709.
36. Krebs, C.J., One hundred years of population ecology: successes, failures and the road ahead. Integr. Zool. 10 (2015), 233–240.
37. Lambert, J.E., Rothman, J.M., 2015. Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Annu. Rev. Anthropol. 44, 493-512.
38. Le Couteur, D.G., Solon-Biet, S., Cogger, V.C., Mitchell, S.J., Senior, A., de Cabo, R., Raubenheimer, D., Simpson, S.J., The impacts of low protein, high carbohydrate diets on ageing and lifespan. Cell. Mol. Life Sci. 73 (2016), 1237–1252.
39. Lee, R.D., Rethinking the evolutionary theory of aging: transfers, not births, shape social species. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 9637–9642.
40. Lee, K.P., Simpson, S.J., Clissold, F.J., Brooks, R., Ballard, J.W.O., Taylor, P.W., Soran, N., Raubenheimer, D., Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 2498–2503.
41. Maklakov, A.A., Simpson, S.J., Zajitschek, F., Hall, M.D., Dessman, J., Clissold, F., Raubenheimer, D., Bonduriansky, R., Brooks, R.C., Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr. Biol. 18 (2008), 1062–1066.
42. Masoro, E.J., Overview of caloric restriction and ageing. Mech. Ageing Dev. 126 (2005), 913–922.
43. Mattson, M.P., Allison, D.B., Fontana, L., Harvie, M., Longo, V.D., Malaisse, W.J., Mosley, M., Notterpek, L., Ravussin, E., Scheer, F.A., Seyfried, T.N., Varady, K.A., Panda, S., Meal frequency and timing in health and disease. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 16647–16653.
44. McCay, C., Crowell, M., Maynard, L., The effect of retarded growth upon the length of life and upon ultimate size. J. Nutr. 10 (1935), 63–79.
45. McLachlan, A.J., Ladle, R.J., Barriers to adaptive reasoning in community ecology. Biol. Rev. 86 (2011), 543–548.
46. Monaghan, P., Charmantier, A., Nussey, D.H., Ricklefs, R.E., The evolutionary ecology of senescence. Funct. Ecol. 22 (2008), 371–378.
47. Nakagawa, S., Lagisz, M., Hector, K.L., Spencer, H.G., Comparative and meta-analytic insights into life-extension via dietary restriction. Aging Cell 11 (2012), 401–409.
48. Nussey, D.H., Froy, H., Lemaitre, J.-F., Gaillard, J.-M., Austad, S.N., Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12 (2013), 214–225.
49. Partridge, L., Gems, D., Beyond the evolutionary theory of ageing, from functional genomics to evo-gero. Trends Ecol. Evol. 21 (2006), 334–340.
50. Piper, M.D.W., Partridge, L., Raubenheimer, D., Simpson, S.J., Dietary restriction and aging: a unifying perspective. Cell Metab. 14 (2011), 154–160.
51. Ponton, F., Wilson, K., Cotter, S.C., Raubenheimer, D., Simpson, S.J., Nutritional immunology: a multi-dimensional approach. PLoS Pathog., 7, 2011, e1002223.
52. Raubenheimer, D., Boggs, C.L., Nutritional ecology, functional ecology and functional ecology. Funct. Ecol. 23 (2009), 1–3.
53. Raubenheimer, D., Simpson, S.J., The geometry of compensatory feeding in the locust. Animal Behaviour 45 (1993), 953–964.
54. Raubenheimer, D., Simpson, S.J., Mayntz, D., Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology 23 (2009), 4–16.
55. Raubenheimer, D., Toward a quantitative nutritional ecology: The right-angled mixture triangle. Ecological Monographs 81 (2011), 407–427.
56. Raubenheimer, D., Simpson, S.J., Integrative models of nutrient balancing: application to insects and vertebrates. Nutr. Res. Rev. 10 (1997), 151–179.
57. Raubenheimer, D., Simpson, S.J., Nutritional ecology and human health. Annu. Rev. Nutr., 36, 2016, 10.1146/annurev-nutr-071715-051118 (in press).
58. Raubenheimer, D., Lee, K.P., Simpson, S.J., Does Bertrand's rule apply to macronutrients?. Proc. R. Soc. B 272 (2005), 2429–2434.
59. Raubenheimer, D., Machovsky-Capuska, G.E., Chapman, C.A., Rothman, J.M., Geometry of nutrition in field studies: an illustration using wild primates. Oecologia 177 (2015), 223–234.
60. Raubenheimer, D., Simpson, S.J., Mayntz, D., Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct. Ecol. 23 (2009), 4–16.
61. Ravussin, E., Redman, L.M., Rochon, J., Das, S.K., Fontana, L., Kraus, W.E., Romashkan, S., Williamson, D.A., Meydani, S.N., Villareal, D.T., Smith, S.R., Stein, R.I., Scott, T.M., Stewart, T.M., Saltzman, E., Klein, S., Bhapkar, M., Martin, C.K., Gilhooly, C.H., Holloszy, J.O., Hadley, E.C., Roberts, S.B., for the CALERIE Study Group, A 2-year randomized controlled trial of human caloric restriction: feasibility and effects on predictors of health span and longevity. J. Gerontol. A Biol. Sci. Med. Sci. 70 (2015), 1097–1104.
62. Remonti, L., Balestrieri, A., Raubenheimer, D., Saino, N., Functional implications of omnivory for dietary nutrient balance. Oikos 000 (2015), 001–008, 10.1111/oik.02801.
63. Rodrigues, M.A., Martins, N.E., Balancé, L.F., Broom, L.N., Dias, A.J., Fernandes, A.S., Rodrigues, F., Sucena, É., Mirth, C.K., Drosophila melanogaster larvae make nutritional choices that minimize developmental time. J. Insect Physiol. 81 (2015), 69–80.
64. Rothman, J.M., Raubenheimer, D., Chapman, C., Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol. Lett. 7 (2011), 847–849.
65. Shokhirev, M.N., Johnson, A.A., Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS One, 9, 2014, e86602.
66. Simpson, S.J., Raubenheimer, D., Feeding behaviour, sensory physiology and nutrient feedback: a unifying model. Entomol. Exp. Appl. 80 (1996), 55–64.
67. Simpson, S.J., Raubenheimer, D., Obesity: the protein leverage hypothesis. Obesity Reviews 6 (2005), 133–142.
68. Simpson, S.J., Raubenheimer, D., A framework for the study of macronutrient intake in fish. Aquac. Res. 32 (2001), 1–12.
69. Simpson, S.J., Raubenheimer, D., Caloric restriction and aging revisited: the need for a geometric analysis of the nutritional bases of aging. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 62 (2007), 707–713.
70. Simpson, S.J., Raubenheimer, D., Macronutrient balance and lifespan. Aging 1 (2009), 875–880.
71. Simpson, S.J., Raubenheimer, D., The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. 2012, Princeton University Press.
72. Simpson, S.J., Le Couteur, D.G., Raubenheimer, D., Putting the balance back in diet. Cell 161 (2015), 18–23.
73. Simpson, S.J., Sibly, R.M., Lee, K.P., Behmer, S.T., Raubenheimer, D., Optimal foraging when regulating intake of multiple nutrients. Anim. Behav. 68 (2004), 1299–1311.
74. Skorupa, D.A., Dervisefendic, A., Zwiener, J., Pletcher, S.D., Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7 (2008), 478–490.
75. Solon-Biet, S.M., Mitchell, S.J., Coogan, S.C.P., Cogger, V.C., Gokam, R., McMahon, A.C., Raubenheimer, D., de Cabo, R., Simpson, S.J., Le Couteur, D.G., Dietary protein to carbohydrate ratio and caloric restriction: comparing metabolic outcomes in mice. Cell Rep. 11 (2015), 1–6.
76. Solon-Biet, S.M., Mitchell, S.J., de Cabo, R., Raubenheimer, D., Le Couteur, D.G., Simpson, S.J., Macronutrients and caloric intake in health and longevity. J. Endocrinol. 226 (2015), R17–R28.
77. Solon-Biet, S.M., Walters, K.A., Simanainen, U.K., McMahon, A.C., Ruohonen, K., Ballard, J.W.O., Raubenheimer, D., Handelsman, D.J., Le Couteur, D.G., Simpson, S.J., Macronutrient balance, reproductive function, and lifespan in ageing mice. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3481–3486.
78. Solon-Biet, S.M., McMahon, A.C., Ballard, W.O., Ruohonen, K., Wu, L.E., Cogger, V.C., Warren, A., Huang, X., Pichaud, N., Melvin, R.G., Gokarn, R., Khalil, M., Turner, N., Cooney, G.J., Sinclair, D.A., Raubenheimer, D., Le Couteur, D.G., Simpson, S.J., The ratio of macronutrients, not caloric intake, dictates cardio metabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab. 19 (2014), 418–430.
79. Speakman, J.R., Mitchell, S.E., Caloric restriction. Mol. Asp. Med. 32 (2011), 159–221.
80. Stroud, J.T., Bush, M.R., Ladd, M.C., Nowicki, R.J., Shantz, A.A., Sweatman, J., Is a community still a community? Reviewing definitions of key terms in community ecology. Ecol. Evol. 5 (2015), 4757–4765.
81. Tait, A.H., Raubenheimer, D., Stockin, K.A., Merriman, M., Machovsky-Capuska, G.E., Nutritional geometry and macronutrient variation in the diets of gannets: the challenges in marine studies. Mar. Biol. 161 (2014), 2791–2801.
82. Warbrick-Smith, J., Raubenheimer, D., Simpson, S.J., Behmer, S.T., Three hundred and fifty generations of extreme food specialization: testing predictions of nutritional ecology. Entomol. Exp. Appl. 132 (2009), 65–75.
83. Zarrinpar, A., Chaix, A., Panda, S., Daily eating patterns and their impact on health and disease. Trends Endocrinol. Metab. 27 (2016), 69–83.