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Nutritional ecology of obesity: from humans to companion animals

  • David Raubenheimer (a1) (a2), Gabriel E. Machovsky-Capuska (a1) (a2), Alison K. Gosby (a1) and Stephen Simpson (a1)

Abstract

We apply nutritional geometry, a framework for modelling the interactive effects of nutrients on animals, to help understand the role of modern environments in the obesity pandemic. Evidence suggests that humans regulate the intake of protein energy (PE) more strongly than non-protein energy (nPE), and consequently will over- and under-ingest nPE on diets with low or high PE, respectively. This pattern of macronutrient regulation has led to the protein leverage hypothesis, which proposes that the rise in obesity has been caused partly by a shift towards diets with reduced PE:nPE ratios relative to the set point for protein regulation. We discuss potential causes of this mismatch, including environmentally induced reductions in the protein density of the human diet and factors that might increase the regulatory set point for protein and hence exacerbate protein leverage. Economics – the high price of protein compared with fats and carbohydrates – is one factor that might contribute to the reduction of dietary protein concentrations. The possibility that rising atmospheric CO2 levels could also play a role through reducing the PE:nPE ratios in plants and animals in the human food chain is discussed. Factors that reduce protein efficiency, for example by increasing the use of ingested amino acids in energy metabolism (hepatic gluconeogenesis), are highlighted as potential drivers of increased set points for protein regulation. We recommend that a similar approach is taken to understand the rise of obesity in other species, and identify some key gaps in the understanding of nutrient regulation in companion animals.

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Corresponding author

* Corresponding author: D. Raubenheimer, email david.raubenheimer@sydney.edu.au

References

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1 Wells, JCK (2006) The evolution of human fatness and susceptibility to obesity: an ethological approach. Biol Rev 81, 183205.
2 Banting, W (1863) Letter on Coruplence, Addressed to the Public. London: Harrison.
3 Bray, GA (2004) The epidemic of obesity and changes in food intake: the fluoride hypothesis. Physiol Behav 82, 115121.
4 Caballero, B (2007) The global epidemic of obesity: an overview. Epidemiol Rev 29, 15.
5 Swinburn, BA, Sacks, G, Hall, KD, et al. (2011) The global obesity pandemic: shaped by global drivers and local environments. Lancet 378, 804814.
6 Haththotuwa, RN, Wijeyaratne, CN & Senarath, U (2013) Worldwide epidemic of obesity. In Obesity: A Ticking Time Bomb for Reproductive Health, pp. 311 [Mahmood, T and Arulkumaran, S, editors]. Oxford: Elsevier.
7 Kanter, R & Caballero, B (2012) Global gender disparities in obesity: a review. Adv Nutr 3, 491498.
8 Popkin, BM, Adair, LS & Ng, SW (2012) Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev 70, 321.
9 Scarlett, JM, Donoghue, S, Saidla, J, et al. (1994) Overweight cats: prevalence and risk factors. Int J Obes Relat Metab Disord 18, S22S28.
10 Zoran, DL (2010) Obesity in dogs and cats: a metabolic and endocrine disorder. Vet Clin North Am Small Anim Pract Mar 40, 221239.
11 German, AJ (2006) The growing problem of obesity in dogs and cats. J Nutr 136, 1940S1946S.
12 Wyse, CA, McNie, KA, Tannahill, VJ, et al. (2008) Prevalence of obesity in riding horses in Scotland. Vet Rec 162, 590591.
13 Giles, SL, Rands, SA, Nicol, CJ, et al. (2014) Obesity prevalence and associated risk factors in outdoor living domestic horses and ponies. Peer J 2, e299.
14 Hebert, JR, Allison, DB, Archer, E, et al. (2013) Scientific decision making, policy decisions, and the obesity pandemic. Mayo Clin Proc 88, 593604.
15 Klimentidis, YC, Beasley, TM, Lin, HY, et al. (2011) Canaries in the coal mine: a cross-species analysis of the plurality of obesity epidemics. Proc Biol Sci 278, 16261632.
16 Raubenheimer, D, Simpson, SJ & Mayntz, D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct Ecol 23, 416.
17 Raubenheimer, D, Simpson, SJ & Tait, AH (2012) Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation. Philos Trans R Soc Lond B Biol Sci 367, 16281646.
18 Simpson, SJ & Raubenheimer, D (2012) The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. Princeton, NJ: Princeton University Press.
19 Raubenheimer, D & Simpson, SJ (1993) The geometry of compensatory feeding in the locust. Anim Behav 45, 953964.
20 Simpson, SJ & Raubenheimer, D (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond B 342, 381402.
21 Simpson, SJ, Batley, R & Raubenheimer, D (2003) Geometric analysis of macronutrient intake in humans: the power of protein? Appetite 41, 123140.
22 Simpson, SJ & Raubenheimer, D (2005) Obesity: the protein leverage hypothesis. Obes Rev 6, 133142.
23 Gosby, AK, Conigrave, AD, Lau, NS, et al. (2011) Testing protein leverage in lean humans: a randomised controlled experimental study. PLoS ONE 6, e25929.
24 Gosby, AK, Conigrave, AD, Raubenheimer, D, et al. (2013) Protein leverage and energy intake. Obes Rev 15, 183191.
25 Foley, R (1995) The adaptive legacy of human evolution: a search for the environment of evolutionary adaptedness. Evol Anthropol 4, 194203.
26 Raubenheimer, D & Simpson, SJ (2010) Hunger and satiety. In Encyclopedia of Animal Behaviour, pp. 117126 [Breed, MD and Moore, J, editors]. Oxford: Academic Press.
27 Simpson, SJ, Sibly, RM, Lee, KP, et al. (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68, 12991311.
28 Raubenheimer, D, Lee, KP & Simpson, SJ (2005) Does Bertrand's rule apply to macronutrients? Proc Biol Sci 272, 24292434.
29 Raubenheimer, D & Simpson, SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10, 151179.
30 Martens, EA, Lemmens, SG & Westerterp-Plantenga, MS (2013) Protein leverage affects energy intake of high-protein diets in humans. Am J Clin Nutr 97, 8693.
31 Food and Nutrition Board (2005) Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The National Academy Press.
32 Astrup, A (2005) The satiating power of protein – a key to obesity prevention? Am J Clin Nutr 82, 12.
33 Larsen, TM, Dalskov, SM, Van Baak, M, et al. (2010) Diets with high or low protein content and glycemic index for weight-loss maintenance. N Engl J Med 363, 21022113.
34 Martinez-Cordero, C, Kuzawa, CW, Sloboda, DM, et al. (2011) Do humans prioritize protein intake? J Dev Orig Health Dis 2, S105.
35 Austin, GL, Ogden, LG & Hill, JO (2011) Trends in carbohydrate, fat, and protein intakes and association with energy intake in normal-weight, overweight, and obese individuals: 1971–2006. J Am Coll Nutr 93, 836843.
36 Monteiro, CA, Moura, EC, Conde, WL, et al. (2004) Socioeconomic status and obesity in adult populations of developing countries: a review. Bull World Health Organ 82, 940946.
37 McLaren, L (2007) Socioeconomic status and obesity. Epidemiol Rev 29, 2948.
38 Dinsa, GD, Goryakin, Y, Fumagalli, E, et al. (2012) Obesity and socioeconomic status in developing countries: a systematic review. Obes Rev 13, 10671079.
39 Jablonka, E & Raz, G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84, 131176.
40 Plotkin, HC & Odling-Smee, FJ (1981) A multiple-level model of evolution and its implications for sociobiology. Behav Brain Sci 4, 225268.
41 Odling-Smee, FJ, Laland, KN & Feldman, MW (2000) Niche construction and gene-culture coevolution: an evolutionary basis for the human sciences (Chapter 4). In Perspectives in Ethology, pp. 89111. New York: Kluwer Academic/Plenum Publishers.
42 Gluckman, PD, Hanson, MA & Spencer, HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20, 527533.
43 Speth, JD & Spielmann, KA (1983) Energy-source, protein-metabolism, and hunter gatherer subsistence strategies. J Anthropol Archaeol 2, 131.
44 Cordain, L, Miller, JB, Eaton, SB, et al. (2000) Macronutrient estimations in hunter–gatherer diets. Am J Clin Nutr 72, 15891590.
45 Konner, M & Eaton, SB (2010) Paleolithic nutrition twenty-five years later. Nutr Clin Pract 25, 594602.
46 Kuipers, RS, Luxwolda, MF, Dijck-Brouwer, DAJ, et al. (2010) Estimated macronutrient and fatty acid intakes from an east African paleolithic diet. Br J Nutr 104, 16661687.
47 Drewnowski, A (1998) Energy density, palatability, and satiety: implications for weight control. Nutr Rev 56, 347353.
48 Raubenheimer, D (2011) Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecol Monogr 81, 407427.
49 Westerterp-Plantenga, MS, Lejeune, MPGM, Nijs, I, et al. (2004) High protein intake sustains weight maintenance after body weight loss in humans. Int J Obes 28, 5764.
50 Weigle, DS, Breen, PA, Matthys, CC, et al. (2005) A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr 82, 4148.
51 Yang, ZY & Huffman, SL (2013) Nutrition in pregnancy and early childhood and associations with obesity in developing countries. Matern Child Nutr 9, 105119.
52 Freckleton, RP, Harvey, PH & Pagel, M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160, 712726.
53 Felton, AM, Felton, A, Raubenheimer, D, et al. (2009) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20, 685690.
54 Felton, AM, Felton, A, Wood, JT, et al. (2009) Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. Int J Primatol 30, 675696.
55 Rothman, JM, Raubenheimer, D & Chapman, CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol Lett 7, 847849.
56 Johnson, CA, Raubenheimer, D, Rothman, JM, et al. (2013) 30 Days in the life: daily nutrient balancing in a wild chacma baboon. PLOS ONE 8, e70383.
57 Irwin, MT, Raharison, JL, Raubenheimer, D, et al. (2013) Nutritional correlates of the “lean season”: effects of seasonality and frugivory on the nutritional ecology of diademed sifakas. Am J Primatol 153, 7891.
58 Cordain, L (1999) Cereal grains: humanity's double-edged sword. In Evolutionary Aspects of Nutrition and Health. Diet, Exercise, Genetics and Chronic Disease, World Rev Nutr Diet, vol. 84, pp. 1973 [Simopoulos, AP, editor]. Basel: Karger.
59 Cordain, L, Watkins, BA, Florant, GL, et al. (2002) Fatty acid analysis of wild ruminant tissues: evolutionary implications for reducing diet-related chronic disease. Eur J Clin Nutr 56, 181191.
60 Mintz, SW (1986) Sweetness and Power. New York: Penguin.
61 Monteiro, CA, Moubarac, JC, Cannon, G, et al. (2013) Ultra-processed products are becoming dominant in the global food system. Obes Rev 14, 2128.
62 Simpson, SJ & Raubenheimer, D (2014) Perspective: tricks of the trade. Nature 508, S66.
63 Langley-Evans, SC (2006) Developmental programming of health and disease. Proc Nutr Soc 65, 97105.
64 Sharp, H, Pickles, A, Meaney, M, et al. (2012) Frequency of infant stroking reported by mothers moderates the effect of prenatal depression on infant behavioural and physiological outcomes. PLOS ONE 7, e45446.
65 Hales, CN & Barker, DJP (1992) Type-2 (on-insulin-dependent) diabetes-mellitus – the thrifty phenotype hypothesis. Diabetologia 35, 595601.
66 Hales, CN & Barker, DJP (2001) The thrifty phenotype hypothesis. Br Med Bull 60, 520.
67 Gluckman, PD & Hanson, MA (2004) The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 15, 183187.
68 Ho, KJ, Mikkelso, B, Lewis, LA, et al. (1972) Alaskan Arctic Eskimo: responses to a customary high fat diet. Am J Clin Nutr 25, 737745.
69 Gadsby, P (2002) The inuit paradox. Discover Magazine 1214.
70 Young, TK (2007) Are the circumpolar Inuit becoming obese? Am J Hum Biol 19, 181189.
71 Galloway, T, Young, TK & Egeland, GM (2010) Emerging obesity among preschool-aged Canadian Inuit children: results from the Nunavut Inuit Child Health Survey. Int J Circumpol Health 69, 151157.
72 Chateau-Degat, M-L, Dewailly, E, Charbonneau, G, et al. (2011) Obesity risks: towards an emerging Inuit pattern. Int J Circumpol Heal 70, 166177.
73 Kuhnlein, HV, Receveur, O, Soueida, R, et al. (2004) Arctic indigenous peoples experience the nutrition transition with changing dietary patterns and obesity. J Nutr 134, 14471453.
74 Günther, ALB, Remer, T, Kroke, A, et al. (2007) Early protein intake and later obesity risk: which protein sources at which time points throughout infancy and childhood are important for body mass index and body fat percentage at 7 y of age? Am J Clin Nutr 86, 17651772.
75 Agostoni, C & Laicini, E (2013) Early exposure to allergens: a new window of opportunity for non-communicable disease prevention in complementary feeding? Int J Food Sci Nutr 65, 12.
76 Hornell, A, Lagstrom, H, Lande, B, et al. (2013) Protein intake from 0 to 18 years of age and its relation to health: a systematic literature review for the 5th Nordic Nutrition Recommendations. Food Nutr Res 57, .
77 Gunther, AL, Remer, T, Kroke, A, et al. (2007) Early protein intake and later obesity risk: which protein sources at which time points throughout infancy and childhood are important for body mass index and body fat percentage at 7 years of age? Am J Clin Nutr 86, 17651772.
78 Weber, M, Grote, V, Closa-Monasterolo, R, et al. (2014) Lower protein content in infant formula reduces BMI and obesity risk at school age: follow-up of a randomized trial. Am J Clin Nutr 99, 10411051.
79 Turner, BL & Thompson, AL (2013) Beyond the Paleolithic prescription: incorporating diversity and flexibility in the study of human diet evolution. Nutr Rev 71, 501510.
80 Wyse, CA, Selman, C, Page, MM, et al. (2011) Circadian desynchrony and metabolic dysfunction; did light pollution make us fat? Med Hypotheses 77, 11391144.
81 Oishi, K & Itoh, N (2013) Disrupted daily light–dark cycle induces the expression of hepatic gluconeogenic regulatory genes and hyperglycemia with glucose intolerance in mice. Biochem Biophys Res Commun 432, 111115.
82 Trickett, EJ & Beehler, S (2013) The ecology of multilevel interventions to reduce social inequalities in health. Am Behav Sci 57, 12271246.
83 Drewnowski, A & Darmon, N (2005) The economics of obesity: dietary energy density and energy cost. Am J Clin Nutr 82, 265S273S.
84 Appelhans, BM, Waring, ME, Schneider, KL, et al. (2012) Delay discounting and intake of ready-to-eat and away-from-home foods in overweight and obese women. Appetite 59, 576584.
85 Pechey, R, Jebb, SA, Kelly, MP, et al. (2013) Socioeconomic differences in purchases of more vs. less healthy foods and beverages: analysis of over 25,000 British households in 2010. Soc Sci Med 92, 2226.
86 Williams, RA, Roe, LS & Rolls, BJ (2013) Comparison of three methods to reduce energy density. Effects on daily energy intake. Appetite 66, 7583.
87 Astrup, A, Kristensen, M, Gregersen, NT, et al. (2010) Can bioactive foods affect obesity? Ann N Y Acad Sci 1190, 2541.
88 Fiszman, S & Varela, P (2013) The satiating mechanisms of major food constituents – an aid to rational food design. Trends Food Sci Technol 32, 4350.
89 Fiszman, S & Varela, P (2013) The role of gums in satiety/satiation. A review. Food Hydrocolloids 32, 147154.
90 Trigueros, L, Pena, S, Ugidos, AV, et al. (2013) Food ingredients as anti-obesity agents: a review. Crit Rev Food Sci Nutr 53, 929942.
91 Brooks, RC, Simpson, SJ & Raubenheimer, D (2010) The price of protein: combining evolutionary and economic analysis to understand excessive energy consumption. Obes Rev 11, 887894.
92 Atwater, WO (1888) Pecuniary economy of food – the chemistry of foods and nutrition V. The Century Magazine 35, 437445.
93 Ruohonen, K, Simpson, SJ & Raubenheimer, D (2007) A new approach to diet optimisation: a re-analysis using European whitefish (Coregonus lavaretus). Aquaculture 267, 147156.
94 Close, RN & Schoeller, DA (2006) The financial reality of overeating. J Am Coll Nutr 25, 203209.
95 IPCC (2013) Fifth Assessment Report. Stockholm/Cambridge: Inter-governmental Panel on Climate Change/Cambridge University Press. www.ipcc.ch (cited 7 June 2013).
96 Robinson, EA, Ryan, GD & Newman, JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194, 321336.
97 Taub, DR, Miller, B & Allen, H (2008) Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis. Glob Change Biol 14, 565575.
98 Hogy, P & Fangmeier, A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. J Cereal Sci 48, 580591.
99 Myers, SS, Zanobetti, A, Kloog, I, et al. (2014) Increasing CO2 threatens human nutrition. Nature 510, 139142.
100 Taub, DR & Wang, X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integr Plant Biol 50, 13651374.
101 Loladze, I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol Evol 17, 457461.
102 Sterner, RW & Elser, JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton, NJ: Princeton University Press.
103 Stafford, N (2007) Future crops – the other greenhouse effect. Nature 448, 526528.
104 Raubenheimer, D & Rothman, JM (2013) The nutritional ecology of entomophagy in humans and other primates. Annu Rev Entomol 58, 141160.
105 Hewson-Hughes, AK, Hewson-Hughes, VL, Miller, AT, et al. (2011) Geometric analysis of macronutrient selection in the adult domestic cat, Felis catus . J Exp Biol 214, 10391051.
106 Plantinga, EA, Bosch, G & Hendriks, WH (2011) Estimation of the dietary nutrient profile of free-roaming feral cats: possible implications for nutrition of domestic cats. Br J Nutr 106, S35S48.
107 Eisert, R (2011) Hypercarnivory and the brain: protein requirements of cats reconsidered. J Comp Physiol B Biocheml Syst Environ Physiol 181, 117.
108 Hewson-Hughes, AK, Hewson-Hughes, VL, Colyer, A, et al. (2013) Consistent proportional macronutrient intake selected by adult domestic cats (Felis catus) despite variations in macronutrient and moisture content of foods offered. J Comp Physiol B Biochem Syst Environ Physiol 183, 525536.
109 Mayntz, D, Raubenheimer, D, Salomon, M, et al. (2005) Nutrient-specific foraging in invertebrate predators. Science 307, 111113.
110 Hewson-Hughes, AK, Hewson-Hughes, VL, Colyer, A, et al. (2013) Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris . Behav Ecol 24, 293304.
111 Erlenbach, JA, Rode, KD, Raubenheimer, D, Robbins, CT (2014) Macronutrient optimization and energy maximization determine diets of brown bears. J Mammal 95, 160168.
112 Axelsson, E, Ratnakumar, A, Arendt, ML, et al. (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495, 360364.
113 Wang, GD, Zhai, WW, Yang, HC, et al. (2013) The genomics of selection in dogs and the parallel evolution between dogs and humans. Nat Commun 4, 1860.
114 Raubenheimer, D, Mayntz, D, Simpson, SJ, et al. (2007) Nutrient-specific compensation following overwintering diapause in a generalist predatory invertebrate: implications for intraguild predation. Ecology 88, 25982608.
115 Mayntz, D, Nielsen, VH, Sorensen, A, et al. (2009) Balancing of protein and lipid by a mammalian carnivore, the mink (Mustela vison). Anim Behav 77, 349355.
116 Farrow, HA, Rand, JS, Morton, JM, et al. (2013) Effect of dietary carbohydrate, fat, and protein on postprandial glycemia and energy intake in cats. J Vet Intern Med 27, 11211135.
117 Courcier, EA, Thomson, RM, Mellor, DJ, et al. (2010) An epidemiological study of environmental factors associated with canine obesity. J Small Anim Pract 51, 362367.
118 Degeling, C, Kerridge, I & Rock, M (2013) What to think of canine obesity? Soc Epistemol 27, 90104.
119 Johnson, PJ, Wiedmeyer, CE, Messer, NT, et al. (2009) Medical implications of obesity in horses – lessons for human obesity. J Diabetes Sci Technol 3, 163174.
120 Eaton, SB & Konner, MJ (1997) Paleolithic nutrition revisited: a twelve-year retrospective on its nature and implications. Eur J Clinl Nutr 51, 207216.
121 Raubenheimer, D, Pontzer, JMH & Simpson, SJ (2013) Macronutrient contributions of insects to the diets of hunter–gatherers: a geometric analysis. J Hum Evol 71, 7076.

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