Advertisement

The Evolution from Lean to Obese State and the Influence of Modern Human Society

  • Eduardo A. Nillni
Chapter

Abstract

One of the paramount changes in human evolution was the development of large brain size with a tremendous impact on the nutritional behavior of our species. A larger brain demands more food intake to keep up with the need of the overall energy budget. This high demand for energy to maintain the brain metabolism forced early humans to move from a strictly vegetarian diet to more energy-rich diet. Changes in nutrient-rich energy diets evolving from an exclusively vegetarian to an omnivorous diet were among many evolutionary factors developed to maintain the high cost of a large human brain. Paleontological data indicates that fast brain evolution occurred with the appearance of Homo erectus 1.8 million years ago, which was related to critical changes in diet, body size, and foraging behavior. Then, the survival of more advanced humans depended on their ability to acquire energy for its daily use and storage, which was well balanced before the advent of modern humans. The energy balance of early humans is disrupted today by an excessive food intake, processed food, and an increase in sedentary life. Obesity pandemic has undoubtedly coincided with not only an increase in unhealthy eating habits but also with migratory movements of different ethnic communities to dissimilar environmental pressures. The heat producing of uncoupling proteins in mitochondria brown adipocyte tissue is believed to be a key driver behind the conquest of a variety of environments in mammals 65 million years ago. This ability to produce and maintain heat contributed to the evolution of mammals to explore and settle in uninhabitable territories throughout the planet by adjusting the thermoregulatory response to sharply different environments. It is also discussed in this chapter several early evolutionary hypotheses to explain the development of obesity and metabolic syndrome, the evolutionary changes from hominoids 20 million years ago to industrialized humans, and the effects on traits causing profound changes in the evolution of human nutritional requirements.

References

  1. Ahima, R. S. (2005). Central actions of adipocyte hormones. Trends in Endocrinology and Metabolism: TEM, 307–313.CrossRefGoogle Scholar
  2. Anton, S. C., Potts, R., & Aiello, L. C. (2014). Human evolution. Evolution of early Homo: An integrated biological perspective. Science, 1236828. https://doi.org/10.1126/science.1236828.
  3. Astrup, A. (1999). Macronutrient balances and obesity: The role of diet and physical activity. Public Health Nutrition, 341–347.Google Scholar
  4. Astrup, A., Toubro, S., Raben, A., & Skov, A. R. (1997). The role of low-fat diets and fat substitutes in body weight management: What have we learned from clinical studies? Journal of the American Dietetic Association, S82–S87.CrossRefPubMedGoogle Scholar
  5. Baschetti, R. (1998). Diabetes epidemic in newly westernized populations: Is it due to thrifty genes or to genetically unknown foods? Journal of the Royal Society of Medicine, 622–625.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bateson, P. (2001). Fetal experience and good adult design. International Journal of Epidemiology, 928–934.CrossRefPubMedGoogle Scholar
  7. Bauer, F., Elbers, C. C., Adan, R. A., Loos, R. J., Onland-Moret, N. C., Grobbee, D. E., van Vliet-Ostaptchouk, J. V., Wijmenga, C., & van der Schouw, Y. T. (2009). Obesity genes identified in genome-wide association studies are associated with adiposity measures and potentially with nutrient-specific food preference. The American Journal of Clinical Nutrition, 951–959. https://doi.org/10.3945/ajcn.2009.27781.CrossRefPubMedGoogle Scholar
  8. Beck-Nielsen, H. (1999). General characteristics of the insulin resistance syndrome: Prevalence and heritability. European Group for the study of Insulin Resistance (EGIR) Drugs, 7–10, 75–82.Google Scholar
  9. Bell, E. A., & Rolls, B. J. (2001). Energy density of foods affects energy intake across multiple levels of fat content in lean and obese women. The American Journal of Clinical Nutrition, 1010–1018.CrossRefPubMedGoogle Scholar
  10. Bellisari, A. (2008). Evolutionary origins of obesity. Obesity Reviews: An Official Journal of the International Association for the Study of Obesity, 165–180. https://doi.org/10.1111/j.1467-789X.2007.00392.x.CrossRefPubMedGoogle Scholar
  11. Berthoud, H. R. (2011). Metabolic and hedonic drives in the neural control of appetite: Who is the boss? Current Opinion in Neurobiology, 888–896. https://doi.org/10.1016/j.conb.2011.09.004.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Berthoud, H. R., & Munzberg, H. (2011). The lateral hypothalamus as integrator of metabolic and environmental needs: From electrical self-stimulation to opto-genetics. Physiology & Behavior, 29–39. https://doi.org/10.1016/j.physbeh.2011.04.051.CrossRefGoogle Scholar
  13. Caballero, B. (2007). The global epidemic of obesity: An overview. Epidemiologic Reviews, 1–5. https://doi.org/10.1093/epirev/mxm012.CrossRefPubMedGoogle Scholar
  14. Chatterjee, H. J., Ho, S. Y., Barnes, I., & Groves, C. (2009). Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evolutionary Biology, 259. https://doi.org/10.1186/1471-2148-9-259.
  15. Clement, K. (2005). Genetics of human obesity. The Proceedings of the Nutrition Society, 133–142.CrossRefPubMedGoogle Scholar
  16. Contreras, C., Novelle, M. G., Leis, R., Dieguez, C., Skrede, S., & Lopez, M. (2013). Effects of neonatal programming on hypothalamic mechanisms controlling energy balance. Hormone and Metabolic Research, 935–944. https://doi.org/10.1055/s-0033-1351281.CrossRefPubMedGoogle Scholar
  17. Cooling, J., & Blundell, J. E. (2001). High-fat and low-fat phenotypes: Habitual eating of high- and low-fat foods not related to taste preference for fat. European Journal of Clinical Nutrition, 1016–1021. https://doi.org/10.1038/sj.ejcn.1601262.CrossRefGoogle Scholar
  18. Cordain, L., Eaton, S. B., Sebastian, A., Mann, N., Lindeberg, S., Watkins, B. A., O'Keefe, J. H., & Brand-Miller, J. (2005). Origins and evolution of the western diet: Health implications for the 21st century. The American Journal of Clinical Nutrition, 341–354.CrossRefPubMedGoogle Scholar
  19. de Krom, M., Bauer, F., Collier, D., Adan, R. A., & la Fleur, S. E. (2009). Genetic variation and effects on human eating behavior. Annual Review of Nutrition, 283–304. https://doi.org/10.1146/annurev-nutr-080508-141124.
  20. Delgado, J. M., & Anand, B. K. (1953). Increase of food intake induced by electrical stimulation of the lateral hypothalamus. The American Journal of Physiology, 162–168.CrossRefGoogle Scholar
  21. DelParigi, A., Pannacciulli, N., Le, D. N., & Tataranni, P. A. (2005a). In pursuit of neural risk factors for weight gain in humans. Neurobiology of Aging, 50–55. https://doi.org/10.1016/j.neurobiolaging.2005.09.008.CrossRefPubMedGoogle Scholar
  22. DelParigi, A., Chen, K., Salbe, A. D., Reiman, E. M., & Tataranni, P. A. (2005b). Sensory experience of food and obesity: A positron emission tomography study of the brain regions affected by tasting a liquid meal after a prolonged fast. NeuroImage, 436–443. https://doi.org/10.1016/j.neuroimage.2004.08.035.
  23. Drewnowski, A. (2003). The role of energy density. Lipids, 109–115.CrossRefPubMedGoogle Scholar
  24. Eaton, S. B. (2006). The ancestral human diet: What was it and should it be a paradigm for contemporary nutrition? The Proceedings of the Nutrition Society, 1–6.CrossRefPubMedGoogle Scholar
  25. Elias, C. F., Aschkenasi, C., Lee, C., Kelly, J., Ahima, R. S., Bjorbaek, C., Flier, J. S., Saper, C. B., & Elmquist, J. K. (1999). Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron, 775–786.CrossRefPubMedGoogle Scholar
  26. Elmquist, J. K., Bjorbaek, C., Ahima, R. S., Flier, J. S., & Saper, C. B. (1998). Distributions of leptin receptor mRNA isoforms in the rat brain. The Journal of Comparative Neurology, 535–547.CrossRefPubMedGoogle Scholar
  27. Flier, J. S. (2004). Obesity wars: Molecular progress confronts an expanding epidemic. Cell, 337–350.CrossRefPubMedGoogle Scholar
  28. Galgani, J., & Ravussin, E. (2008). Energy metabolism, fuel selection and body weight regulation. International Journal of Obesity, (2005), S109–S119. https://doi.org/10.1038/ijo.2008.246.CrossRefPubMedGoogle Scholar
  29. Garn, S. M., & Leonard, W. R. (1989). What did our ancestors eat? Nutrition Reviews, 337–345.CrossRefGoogle Scholar
  30. Genne-Bacon, E. A. (2014). Thinking evolutionarily about obesity. The Yale Journal of Biology and Medicine, 99–112.Google Scholar
  31. Gluckman, P. D., & Hanson, M. A. (2006). Evolution, development and timing of puberty. Trends in endocrinology and metabolism: TEM, 7–12. https://doi.org/10.1016/j.tem.2005.11.006.CrossRefGoogle Scholar
  32. Gonzalez, R., Sarr, M. G., Smith, C. D., Baghai, M., Kendrick, M., Szomstein, S., Rosenthal, R., & Murr, M. M. (2007). Diagnosis and contemporary management of anastomotic leaks after gastric bypass for obesity. Journal of the American College of Surgeons, 47–55. https://doi.org/10.1016/j.jamcollsurg.2006.09.023.CrossRefPubMedGoogle Scholar
  33. Gotoh, K., Fukagawa, K., Fukagawa, T., Noguchi, H., Kakuma, T., Sakata, T., & Yoshimatsu, H. (2005). Glucagon-like peptide-1, corticotropin-releasing hormone, and hypothalamic neuronal histamine interact in the leptin-signaling pathway to regulate feeding behavior. The FASEB Journal, 1131–1133. https://doi.org/10.1096/fj.04-2384fje.CrossRefPubMedGoogle Scholar
  34. Hales, C. N., & Barker, D. J. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia, 595–601.CrossRefPubMedGoogle Scholar
  35. Holzapfel, C., Grallert, H., Huth, C., Wahl, S., Fischer, B., Doring, A., Ruckert, I. M., Hinney, A., Hebebrand, J., Wichmann, H. E., Hauner, H., Illig, T., & Heid, I. M. (2010). Genes and lifestyle factors in obesity: Results from 12,462 subjects from MONICA/KORA. International Journal of Obesity, (2005), 1538–1545. https://doi.org/10.1038/ijo.2010.79.CrossRefPubMedGoogle Scholar
  36. Hommel, J. D., Trinko, R., Sears, R. M., Georgescu, D., Liu, Z. W., Gao, X. B., Thurmon, J. J., Marinelli, M., & DiLeone, R. J. (2006). Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron, 801–810. https://doi.org/10.1016/j.neuron.2006.08.023.CrossRefPubMedGoogle Scholar
  37. Isler, K., & van Schaik, C. P. (2012). Allomaternal care, life history and brain size evolution in mammals. Journal of Human Evolution, 63, 52. https://doi.org/10.1016/j.jhevol.2012.03.009.CrossRefPubMedGoogle Scholar
  38. Jensen, M. D. (2008). Role of body fat distribution and the metabolic complications of obesity. The Journal of Clinical Endocrinology and Metabolism, S57–S63. https://doi.org/10.1210/jc.2008-1585.
  39. Keski-Rahkonen, A., Kaprio, J., Rissanen, A., Virkkunen, M., & Rose, R. J. (2003). Breakfast skipping and health-compromising behaviors in adolescents and adults. European Journal of Clinical Nutrition, 842–853. https://doi.org/10.1038/sj.ejcn.1601618.CrossRefPubMedGoogle Scholar
  40. Kim, J. G., Suyama, S., Koch, M., Jin, S., Argente-Arizon, P., Argente, J., Liu, Z. W., Zimmer, M. R., Jeong, J. K., Szigeti-Buck, K., Gao, Y., Garcia-Caceres, C., Yi, C. X., Salmaso, N., Vaccarino, F. M., Chowen, J., Diano, S., Dietrich, M. O., Tschop, M. H., & Horvath, T. L. (2014). Leptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding. Nature Neuroscience, 908–910. https://doi.org/10.1038/nn.3725.CrossRefPubMedGoogle Scholar
  41. Koch, M., Varela, L., Kim, J. G., Kim, J. D., Hernandez-Nuno, F., Simonds, S. E., Castorena, C. M., Vianna, C. R., Elmquist, J. K., Morozov, Y. M., Rakic, P., Bechmann, I., Cowley, M. A., Szigeti-Buck, K., Dietrich, M. O., Gao, X. B., Diano, S., & Horvath, T. L. (2015). Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature, 45–50. https://doi.org/10.1038/nature14260.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Leonard, W. R. (2002). Food for thought. Dietary change was a driving force in human evolution. Scientific American, 106–115.CrossRefPubMedGoogle Scholar
  43. Leonard, W. R., & Robertson, M. L. (1992). Nutritional requirements and human evolution: A bioenergetics model. American Journal of Human Biology: Official Journal of the Human Biology Council, 179–195. https://doi.org/10.1002/ajhb.1310040204.CrossRefPubMedGoogle Scholar
  44. Leonard, W. R., & Robertson, M. L. (1994). Evolutionary perspectives on human nutrition: The influence of brain and body size on diet and metabolism. American Journal of Human Biology: Official Journal of the Human Biology Council, 77–88. https://doi.org/10.1002/ajhb.1310060111.CrossRefPubMedGoogle Scholar
  45. Leonard, W. R., Sorensen, M. V., Galloway, V. A., Spencer, G. J., Mosher, M. J., Osipova, L., & Spitsyn, V. A. (2002). Climatic influences on basal metabolic rates among circumpolar populations. American Journal of Human Biology: The Official Journal of the Human Biology Council, 609–620. https://doi.org/10.1002/ajhb.10072.CrossRefPubMedGoogle Scholar
  46. Leonard, W. R., Snodgrass, J. J., & Robertson, M. L. (2007). Effects of brain evolution on human nutrition and metabolism. Annual Review of Nutrition, 27, 311. https://doi.org/10.1146/annurev.nutr.27.061406.093659.CrossRefPubMedGoogle Scholar
  47. Lowell, B. B., & Spiegelman, B. M. (2000). Towards a molecular understanding of adaptive thermogenesis. Nature, 652–660. https://doi.org/10.1038/35007527.CrossRefPubMedGoogle Scholar
  48. Ludwig, D. S., Tritos, N. A., Mastaitis, J. W., Kulkarni, R., Kokkotou, E., Elmquist, J., Lowell, B., Flier, J. S., & Maratos-Flier, E. (2001). Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. The Journal of Clinical Investigation, 379–386. https://doi.org/10.1172/JCI10660.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Malik, S., McGlone, F., Bedrossian, D., & Dagher, A. (2008). Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metabolism, 400–409. https://doi.org/10.1016/j.cmet.2008.03.007.CrossRefPubMedGoogle Scholar
  50. Murray, S., Tulloch, A., Gold, M. S., & Avena, N. M. (2014). Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nature Reviews Endocrinology, 540–552. https://doi.org/10.1038/nrendo.2014.91.CrossRefPubMedGoogle Scholar
  51. Narayanan, N. S., Guarnieri, D. J., & DiLeone, R. J. (2010). Metabolic hormones, dopamine circuits, and feeding. Frontiers in Neuroendocrinology, 104–112. https://doi.org/10.1016/j.yfrne.2009.10.004.CrossRefPubMedGoogle Scholar
  52. Neel, J. V. (1962). Diabetes mellitus: A "thrifty" genotype rendered detrimental by "progress"? American Journal of Human Genetics, 353–362.Google Scholar
  53. Neel, J. V. (1999). The "thrifty genotype" in 1998. Nutrition Reviews, S2–S9.Google Scholar
  54. Nillni, E. A. (2010). Regulation of the hypothalamic thyrotropin releasing hormone (TRH) neuron by neuronal and peripheral inputs. Frontiers in Neuroendocrinology, 134–156. doi: S0091-3022(10)00002-6 [pii]. https://doi.org/10.1016/j.yfrne.2010.01.001.
  55. Nillni, E. A., & Sevarino, K. A. (1999). The biology of pro-thyrotropin-releasing hormone-derived peptides. Endocrine Reviews, 599–648.PubMedGoogle Scholar
  56. Obesity: preventing and managing the global epidemic. (2000). Report of a WHO consultation. World Health Organization technical report series:i–xii, 1–253.Google Scholar
  57. Oelkrug, R., Goetze, N., Exner, C., Lee, Y., Ganjam, G. K., Kutschke, M., Muller, S., Stohr, S., Tschop, M. H., Crichton, P. G., Heldmaier, G., Jastroch, M., & Meyer, C. W. (2013). Brown fat in a protoendothermic mammal fuels eutherian evolution. Nature Communications, 2140. https://doi.org/10.1038/ncomms3140.
  58. Olds, J., & Milner, P. (1954). Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. Journal of Comparative and Physiological Psychology, 419–427.CrossRefPubMedGoogle Scholar
  59. O'Rahilly, S., & Farooqi, I. S. (2006). Genetics of obesity. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 1095–1105. https://doi.org/10.1098/rstb.2006.1850.CrossRefGoogle Scholar
  60. Perello, M., Stuart, R. C., & Nillni, E. A. (2006). The role of intracerebroventricular administration of leptin in the stimulation of prothyrotropin releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology, 3296–3306.CrossRefPubMedGoogle Scholar
  61. Pomp, D., & Mohlke, K. L. (2008). Obesity genes: So close and yet so far. Journal of Biology, 36. https://doi.org/10.1186/jbiol93.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pontzer, H., Brown, M. H., Raichlen, D. A., Dunsworth, H., Hare, B., Walker, K., Luke, A., Dugas, L. R., Durazo-Arvizu, R., Schoeller, D., Plange-Rhule, J., Bovet, P., Forrester, T. E., Lambert, E. V., Thompson, M. E., Shumaker, R. W., & Ross, S. R. (2016a). Metabolic acceleration and the evolution of human brain size and life history. Nature, 390–392. https://doi.org/10.1038/nature17654.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pontzer, H., Durazo-Arvizu, R., Dugas, L. R., Plange-Rhule, J., Bovet, P., Forrester, T. E., Lambert, E. V., Cooper, R. S., Schoeller, D. A., & Luke, A. (2016b). Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Current Biology, 410–417. https://doi.org/10.1016/j.cub.2015.12.046.CrossRefPubMedGoogle Scholar
  64. Prentice, A. M. (2001). Obesity and its potential mechanistic basis. British Medical Bulletin, 51–67.CrossRefPubMedGoogle Scholar
  65. Rui, L. (2013). Brain regulation of energy balance and body weight. Reviews in Endocrine & Metabolic Disorders, 387–407. https://doi.org/10.1007/s11154-013-9261-9.CrossRefPubMedGoogle Scholar
  66. Saito, S., Saito, C. T., & Shingai, R. (2008). Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene, 37–44. https://doi.org/10.1016/j.gene.2007.10.018.CrossRefPubMedGoogle Scholar
  67. Sanchez, V. C., Goldstein, J., Stuart, R. C., Hovanesian, V., Huo, L., Munzberg, H., Friedman, T. C., Bjorbaek, C., & Nillni, E. A. (2004). Regulation of hypothalamic prohormone convertases 1 and 2 and effects on processing of prothyrotropin-releasing hormone. The Journal of Clinical Investigation, 357–369.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Saper, C. B., Chou, T. C., & Elmquist, J. K. (2002). The need to feed: Homeostatic and hedonic control of eating. Neuron, 199–211.CrossRefPubMedGoogle Scholar
  69. Schuppli, C., Isler, K., & van Schaik, C. P. (2012). How to explain the unusually late age at skill competence among humans. Journal of Human Evolution, 843–850. https://doi.org/10.1016/j.jhevol.2012.08.009.CrossRefPubMedGoogle Scholar
  70. Sellayah, D., Cagampang, F. R., & Cox, R. D. (2014). On the evolutionary origins of obesity: A new hypothesis. Endocrinology, 1573–1588. https://doi.org/10.1210/en.2013-2103.CrossRefPubMedGoogle Scholar
  71. Sorensen, T. I., Price, R. A., Stunkard, A. J., & Schulsinger, F. (1989). Genetics of obesity in adult adoptees and their biological siblings. BMJ, 87–90.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Speakman, J. R. (2006). Thrifty genes for obesity and the metabolic syndrome--time to call off the search? Diabetes & Vascular Disease Research, 7–11. https://doi.org/10.3132/dvdr.2006.010.CrossRefPubMedGoogle Scholar
  73. Speakman, J. R. (2008). Thrifty genes for obesity, an attractive but flawed idea, and an alternative perspective: The 'drifty gene' hypothesis. International Journal of Obesity, (2005), 1611–1617. https://doi.org/10.1038/ijo.2008.161.CrossRefPubMedGoogle Scholar
  74. Speiser, D. I., Lampe, R. I., Lovdahl, V. R., Carrillo-Zazueta, B., Rivera, A. S., & Oakley, T. H. (2013). Evasion of predators contributes to the maintenance of male eyes in sexually dimorphic Euphilomedes ostracods (Crustacea). Integrative and Comparative Biology, 78–88. https://doi.org/10.1093/icb/ict025.CrossRefPubMedGoogle Scholar
  75. Spence, R., Wootton, R. J., Barber, I., Przybylski, M., & Smith, C. (2013). Ecological causes of morphological evolution in the three-spined stickleback. Ecology and Evolution, 1717–1726. https://doi.org/10.1002/ece3.581.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Stoger, R. (2008). The thrifty epigenotype: An acquired and heritable predisposition for obesity and diabetes? BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 156–166. https://doi.org/10.1002/bies.20700.CrossRefPubMedGoogle Scholar
  77. Stuber, G. D., & Wise, R. A. (2016). Lateral hypothalamic circuits for feeding and reward. Nature Neuroscience, 198–205. https://doi.org/10.1038/nn.4220.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Stunkard, A. J., Berkowitz, R. I., Stallings, V. A., & Schoeller, D. A. (1999). Energy intake, not energy output, is a determinant of body size in infants. The American Journal of Clinical Nutrition, 524–530.CrossRefPubMedGoogle Scholar
  79. Tataranni, P. A., Harper, I. T., Snitker, S., Del Parigi, A., Vozarova, B., Bunt, J., Bogardus, C., & Ravussin, E. (2003). Body weight gain in free-living pima Indians: Effect of energy intake vs expenditure. International Journal of Obesity and Related Metabolic Disorders: Journal of the International Association for the Study of Obesity, 1578–1583. https://doi.org/10.1038/sj.ijo.0802469.CrossRefPubMedGoogle Scholar
  80. van Schaik, C. P., Isler, K., & Burkart, J. M. (2012). Explaining brain size variation: From social to cultural brain. Trends in Cognitive Sciences, 277–284. https://doi.org/10.1016/j.tics.2012.04.004.
  81. van Woerden, J. T., Willems, E. P., van Schaik, C. P., & Isler, K. (2012). Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution: International Journal of Organic Evolution, 191–199. https://doi.org/10.1111/j.1558-5646.2011.01434.x.
  82. Volkow, N. D., & Wise, R. A. (2005). How can drug addiction help us understand obesity? Nature Neuroscience, 555–560. https://doi.org/10.1038/nn1452.CrossRefPubMedGoogle Scholar
  83. Waterson, M. J., & Horvath, T. L. (2015). Neuronal regulation of energy homeostasis: Beyond the hypothalamus and feeding. Cell Metabolism, 962–970. https://doi.org/10.1016/j.cmet.2015.09.026.CrossRefPubMedGoogle Scholar
  84. Watve, M. G., & Yajnik, C. S. (2007). Evolutionary origins of insulin resistance: A behavioral switch hypothesis. BMC Evolutionary Biology, 61. https://doi.org/10.1186/1471-2148-7-61.
  85. Wells, J. C. (2007). Environmental quality, developmental plasticity and the thrifty phenotype: A review of evolutionary models. Evolutionary Bioinformatics Online, 109–120.Google Scholar
  86. Weyer, C., Snitker, S., Bogardus, C., & Ravussin, E. (1999). Energy metabolism in African Americans: Potential risk factors for obesity. The American Journal of Clinical Nutrition, 13–20.CrossRefPubMedGoogle Scholar
  87. Willett, W. C., & Leibel, R. L. (2002). Dietary fat is not a major determinant of body fat. The American Journal of Medicine, 47S–59S.Google Scholar
  88. Wong, W. W., Butte, N. F., Ellis, K. J., Hergenroeder, A. C., Hill, R. B., Stuff, J. E., & Smith, E. O. (1999). Pubertal African-American girls expend less energy at rest and during physical activity than Caucasian girls. The Journal of Clinical Endocrinology and Metabolism, 906–911. https://doi.org/10.1210/jcem.84.3.5517.Google Scholar
  89. Woods, S. C., & Seeley, R. J. (2000). Adiposity signals and the control of energy homeostasis. Nutrition, 894–902.CrossRefPubMedGoogle Scholar
  90. Yu, Y. H., Vasselli, J. R., Zhang, Y., Mechanick, J. I., Korner, J., & Peterli, R. (2015). Metabolic vs. hedonic obesity: A conceptual distinction and its clinical implications. Obesity Reviews : An Official Journal of the International Association for the Study of Obesity, 234–247. https://doi.org/10.1111/obr.12246.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Emeritus Professor of Medicine, Molecular Biology, Cell Biology & Biochemistry, Department of Medicine, Molecular Biology, Cell Biology & BiochemistryThe Warren Alpert Medical School of Brown UniversityProvidenceUSA

Personalised recommendations