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Adipose Tissue in Evolution

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Adipose Tissue and Adipokines in Health and Disease

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Abstract

For storage and later utilization of ingested energy, fat is the most efficient form, because 1 g of fat contains nine calories, whereas 1 g of protein or carbohydrates contains only four calories. Ever since Neel’s [60] concept of a “thrifty genotype,” the human ability to store fat in adipose depots has been related to our species’ potential to withstand periodic famines. This ability, while being adaptive for subsistence cultures in a rough and highly variable Pleistocene environment, has become a maladaptation in modern societies due to the continuous availability of the preferred sweet and fatty foods. To understand the recent global trend toward obesity in humans, we need an evolutionary perspective on the costs and benefits of adipose depots (cf. [10, 68, 84]), which can be gained by looking at other mammals and, in particular, primates. Many animals living in natural habitats manage to meet the challenge of alternating periods of food scarcity and abundance by storing fat. Others rely more on skillful retrieval and extraction of hidden high-quality foods, and thus follow a strategy of cognitive instead of physiological flexibility. In this chapter, I will present comparative evidence for an almost unique human strategy to combine physiological and cognitive buffering of lean periods.

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References

  1. Aiello LC, Key C. Energetic consequences of being a Homo erectus female. Am J Hum Biol. 2002;14(5):551–65.

    Article  PubMed  Google Scholar 

  2. Aiello LC, Wells JCK. Energetics and the evolution of the genus Homo. Ann Rev Anthropol. 2002;31:323–38.

    Article  Google Scholar 

  3. Aiello LC, Wheeler P. The expensive-tissue hypothesis—the brain and the digestive-system in human and primate evolution. Curr Anthropol. 1995;36(2):199–221.

    Article  Google Scholar 

  4. Aiello LC, Bates N, Joffe T. In defense of the expensive tissue hypothesis. In: Falk D, Gibson KR, editors. Evolutionary Anatomy of the Primate Cerebral Cortex. Cambridge: Cambridge University Press; 2001. p. 57–78.

    Chapter  Google Scholar 

  5. Alexander RM. Principles of Animal Locomotion. Princeton: Princeton University Press; 2003.

    Google Scholar 

  6. Altmann J, Schoeller D, Altmann SA, Muruthi P, Sapolsky RM. Body size and fatness of free-living baboons reflect food availability and activity levels. Am J Primatol. 1993;10:149–61.

    Article  Google Scholar 

  7. Barrickman NL, Lin MJ. Encephalization, expensive tissues, and energetics: an examination of the relative costs of brain size in strepsirrhines. Am J Phys Anthropol. 2010;143(4):579–90.

    Article  PubMed  Google Scholar 

  8. Barrickman NL, Bastian ML, Isler K, van Schaik CP. Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J Hum Evol. 2008;54(5):568–90.

    Article  PubMed  Google Scholar 

  9. Battley PF, Piersma T, Dietz MW, Tang SX, Dekinga A, Hulsman K. Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc R Soc Lond B Biol Sci. 2000;267(1439):191–5.

    Article  CAS  Google Scholar 

  10. Bellisari A. Evolutionary origins of obesity. Obes Rev. 2008;9(2):165–80.

    Article  CAS  PubMed  Google Scholar 

  11. Berger LR, de Ruiter DJ, Churchill SE, Schmid P, Carlson KJ, Dirks PHGM, et al. Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science. 2010;328:195–204.

    Article  CAS  PubMed  Google Scholar 

  12. Boogert NJ, Fawcett TW, Lefebvre L. Mate choice for cognitive traits: a review of the evidence in nonhuman vertebrates. Behav Ecol. 2011;22(3):447–59.

    Article  Google Scholar 

  13. Bousquet-Mélou A, Galitzky J, Lafontan M, Berlan M. Control of lypolysis in intra-abdominal fat cells of nonhuman primates: comparison with humans. J Lipid Res. 1995;36:451–61.

    PubMed  Google Scholar 

  14. Capellini I, Venditti C, Barton RA. Placentation and maternal investment in mammals. Am Nat. 2011;177(1):86–98.

    Article  PubMed  Google Scholar 

  15. Comuzzie AG, Cole SA, Martin L, Carey KD, Mahaney MC, Blangero J, VandeBerg JL. The baboon as a nonhuman primate model for the study of the genetics of obesity. Obes Res. 2003;11:75–80.

    Article  PubMed  Google Scholar 

  16. Cunnane SC, Crawford MA. Survival of the fattest: fat babies were the key to evolution of the large human brain. Comp Biochem Physiol A. 2003;136(1):17–26.

    Article  Google Scholar 

  17. Deaner RO, Isler K, Burkart JM, van Schaik CP. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav Evol. 2007;70:115–24.

    Article  PubMed  Google Scholar 

  18. DeSilva JM, Lesnik JJ. Brain size at birth throughout human evolution: a new method for estimating neonatal brain size in hominins. J Hum Evol. 2008;55(6):1064–74.

    Article  PubMed  Google Scholar 

  19. Dierenfeld ES. Orangutan nutrition. In: Sodaro C, editor. Orangutan SSP Husbandry Manual. Brookfield, IL: Orangutan SSP; 1997. p. 115–21.

    Google Scholar 

  20. Donges JF, Donner RV, Trauth MH, Marwan N, Schellnhuber HJ, Kurths J. Nonlinear detection of paleoclimate-variability transitions possibly related to human evolution. Proc Natl Acad Sci U S A. 2011;108(51):20422–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Dufour DL, Sauther ML. Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am J Hum Biol. 2002;14(5):584–602.

    Article  CAS  PubMed  Google Scholar 

  22. Emery Thompson M, Muller MN, Wrangham RW, Lwanga JS, Potts KB. Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav. 2009;55(2):299–305.

    Article  PubMed  Google Scholar 

  23. Ellison PT. On Fertile Ground: A Natural History of Human Reproduction. Cambridge: Harvard University Press; 2001.

    Google Scholar 

  24. Erren TC, Erren M. Can fat explain the human brain’s big bang evolution?—Horrobin’s leads for comparative and functional genomics. Prostaglandins Leukot Essent Fatty Acids. 2004;70:345–7.

    Article  CAS  PubMed  Google Scholar 

  25. Falk D, Hildebolt C, Smith K, Morwood MJ, Sutikna T, Brown P, et al. The brain of LB1, Homo floresiensis. Science. 2005;308(5719):242–5.

    Article  CAS  PubMed  Google Scholar 

  26. Farquharson J, Jamieson E, Logan R, Cockburn F, Ainslie PW. Infant cerebral cortex phospholipid fatty-acid composition and diet. Lancet. 1992;340(8823):810–3.

    Article  CAS  PubMed  Google Scholar 

  27. Foley RA, Lee PC. Ecology and energetics of encephalization in hominid evolution. Phil Trans R Soc Lond B-Biol Sci. 1991;334(1270):223–32.

    Article  CAS  Google Scholar 

  28. Gonzalez-Lagos C, Sol D, Reader SM. Large-brained mammals live longer. J Evol Biol. 2010;23:1064–74.

    Article  CAS  PubMed  Google Scholar 

  29. Hartwig W, Rosenberger AL, Norconk MA, Owl MY. Relative brain size, gut size, and evolution in New World monkeys. Anat Rec. 2011;294(12):2207–21.

    Article  Google Scholar 

  30. Hawkes K, O’Connell JF, Blurton Jones NG, Alvarez H, Charnov EL. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci U S A. 1998;95(3):1336–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Healy SD, Rowe C. A critique of comparative studies of brain size. Proc R Soc Lond B Biol Sci. 2007;274(1609):453–64.

    Article  Google Scholar 

  32. Heldmaier G, Ortmann S, Elvert R. Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol. 2004;141(3):317–29.

    Article  PubMed  Google Scholar 

  33. Howard Jr CF, editor. Nonhuman primate studies on diabetes, carbohydrate intolerance, and obesity. New York: Alan R. Liss; 1988.

    Google Scholar 

  34. Isler K, van Schaik CP. Costs of encephalisation: the energy trade-off hypothesis tested on birds. J Hum Evol. 2006;51(3):228–43.

    Article  PubMed  Google Scholar 

  35. Isler K, van Schaik CP. Metabolic costs of brain size evolution. Biol Lett. 2006;2(4):557–60.

    Article  PubMed Central  PubMed  Google Scholar 

  36. Isler K, van Schaik CP. The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol. 2009;57(4):392–400.

    Article  PubMed  Google Scholar 

  37. Isler K, van Schaik CP. Allomaternal care, life history and brain size evolution in mammals. J Hum Evol. 2012;63(1):52–63.

    Article  PubMed  Google Scholar 

  38. Isler K, van Schaik CP. How our ancestors broke through the gray ceiling: comparative evidence for cooperative breeding in early Homo. Curr Anthropol. 2012;53(S6):S453–65.

    Google Scholar 

  39. Jones KE, MacLarnon AM. Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am Nat. 2004;164(1):E20–31.

    Article  PubMed  Google Scholar 

  40. Kaplan H, Hill K, Lancaster J, Hurtado AM. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol. 2000;9(4):156–85.

    Article  Google Scholar 

  41. Kappelman J. The evolution of body mass and relative brain size in fossil hominids. J Hum Evol. 1996;30:243–76.

    Article  Google Scholar 

  42. Kaufman JA, Hladik CM, Pasquet P. On the expensive-tissue hypothesis: independent support from highly encephalized fish. Curr Anthropol. 2003;44(5):705–7.

    Article  Google Scholar 

  43. Keagy J, Savard JF, Borgia G. Complex relationship between multiple measures of cognitive ability and male mating success in satin bowerbirds, Ptilonorhynchus violaceus. Anim Behav. 2011;81(5):1063–70.

    Article  Google Scholar 

  44. Kleiber M. The Fire of Life: An Introduction to Animal Energetics. New York: John Wiley; 1961.

    Google Scholar 

  45. Knott CD. Changes in orangutan diet, calorie intake and ketones in response to fluctuating fruit availability. Int J Primatol. 1998;19:1061–79.

    Article  Google Scholar 

  46. Kuzawa CW. Adipose tissue in human infancy and childhood: an evolutionary perspective. Am J Phys Anthropol. 1998;41:177–209.

    Article  Google Scholar 

  47. Lawrence M, Coward W, Lawrence F, Cole T, Whitehead R. Fat gain during pregnancy in rural African women: the effect of season and dietary status. Am J Clin Nutr. 1987;45:1442–50.

    CAS  PubMed  Google Scholar 

  48. Leendertz SAJ, Metzger S, Skjerve E, Deschner T, Boesch C, Riedel J, et al. A longitudinal study of urinary dipstick parameters in wild chimpanzees (Pan troglodytes verus) in Côte d’Ivoire. Am J Primatol. 2010;71:1–10.

    Google Scholar 

  49. Leigh S. Relations between captive and noncaptive weights in anthropoid primates. Zoo Biol. 1994;13:21–43.

    Article  Google Scholar 

  50. Leonard WR, Robertson ML, Snodgrass JJ, Kuzawa CW. Metabolic correlates of hominid brain evolution. Comp Biochem Physiol A. 2003;136(1):5–15.

    Article  Google Scholar 

  51. Lovejoy CO. Reexamining human origins in light of Ardipithecus ramidus. Science. 2009;326(5949):74e1–8.

    PubMed  Google Scholar 

  52. Lukas WD, Campbell BC. Evolutionary and ecological aspects of early brain malnutrition in humans. Hum Nat. 2000;11:1–26.

    Article  Google Scholar 

  53. Mahan DC, Watts MR, St-Pierre N. Macro- and micromineral composition of fetal pigs and their accretion rates during fetal development. J Anim Sci. 2009;87(9):2823–32.

    Article  CAS  PubMed  Google Scholar 

  54. Maquet P. Sleep function(s) and cerebral metabolism. Behav Brain Res. 2000;69(1–2):75–83.

    Google Scholar 

  55. Martin RD. The evolution of human reproduction: a primatological perspective. Am J Phys Anthropol. 2007;45:59–84.

    Article  PubMed  Google Scholar 

  56. McNab BK. An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A. 2008;151(1):5–28.

    Article  Google Scholar 

  57. Milligan LA, Rapoport SI, Cranfield MR, Dittus W, Glander KE, Oftedal OT, et al. Fatty acid composition of wild anthropoid primate milks. Comp Biochem Physiol B: Biochem Mol Biol. 2008;149(1):74–82.

    Article  Google Scholar 

  58. Muller AE. Aspects of social life in the fat-tailed dwarf lemur (Cheirogaleus medius): Inferences from body weights and trapping data. Am J Primatol. 1999;49(3):265–80.

    Article  CAS  PubMed  Google Scholar 

  59. Navarrete AF, van Schaik CP, Isler K. Energetics and the evolution of human brain size. Nature. 2011;480:91–3.

    Article  CAS  PubMed  Google Scholar 

  60. Neel JV. Diabetes mellitus—a thrifty genotype rendered detrimental by progress. Am J Hum Genet. 1962;14:353–62.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Norgan NG. Population differences in body composition in relation to the body mass index. Eur J Clin Nutr. 1994;48(S3):S10–25.

    PubMed  Google Scholar 

  62. Nunn CL. The Comparative Approach in Evolutionary Anthropology and Biology. Chicago, IL: University of Chicago Press; 2011.

    Book  Google Scholar 

  63. Pereira ME, Pond CM. Organization of white adipose tissue in Lemuridae. Am J Primatol. 1995;35(1):1–13.

    Article  Google Scholar 

  64. Pond CM. The biological origins of adipose tissue in humans. In: Morbeck M, Galloway A, Zihlman A, editors. The Evolving Female: A Life-history Perspective. Princeton: Princeton University Press; 1997. p. 147–62.

    Google Scholar 

  65. Pond CM. The Fats of Life. Cambridge, UK: Cambridge University Press; 1998.

    Book  Google Scholar 

  66. Pond CM, Mattacks CA. The anatomy of adipose tissue in captive Macaca monkeys and its implications for human biology. Folia Primatol. 1987;48(3–4):164–85.

    Article  CAS  PubMed  Google Scholar 

  67. Pontzer H, Rolian C, Rightmire GP, Jashashvili T, de Leon MSP, Lordkipanidze D, et al. Locomotor anatomy and biomechanics of the Dmanisi hominins. J Hum Evol. 2010;58(6):492–504.

    Article  PubMed  Google Scholar 

  68. Power ML, Schulkin J. The Evolution of Obesity. Baltimore, ML: Johns Hopkins University Press; 2009.

    Google Scholar 

  69. Power ML, Ross CN, Schulkin J, Tardif SD. The development of obesity begins at an early age in captive common marmosets (Callithrix jacchus). Am J Primatol. 2012;74(3):261–9.

    Article  PubMed Central  PubMed  Google Scholar 

  70. Rightmire GP, Lordkipanidze D, Vekua A. Anatomical descriptions, comparative studies and evolutionary significance of the hominin skulls from Dmanisi, Republic of Georgia. J Hum Evol. 2006;50(2):115–41.

    Article  PubMed  Google Scholar 

  71. Rivers JPW. The biology of famine. In: Harrison GA, editor. Famine. Oxford: Oxford University Press; 1988. p. 1–108.

    Google Scholar 

  72. Rolfe DFS, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 1997;77(3):731–58.

    CAS  PubMed  Google Scholar 

  73. Schmid J, Speakman JR. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests. Naturwissenschaften. 2009;96(5):609–20.

    Article  CAS  PubMed  Google Scholar 

  74. Schwartz SM, Kemnitz JW. Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques. Am J Phys Anthropol. 1992;89:109–21.

    Article  CAS  PubMed  Google Scholar 

  75. Setchell JM, Dixson AF. Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx). Am J Phys Anthropol. 2001;115:245–52.

    Article  CAS  PubMed  Google Scholar 

  76. Sol D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett. 2009;5(1):130–3.

    Article  PubMed Central  PubMed  Google Scholar 

  77. Speijer D. Brains have a gut feeling about fat storage. BioEssays. 2012;34:275–6.

    Article  PubMed  Google Scholar 

  78. Trayhum P. Endcrine and signalling role of adipose tissue: new perspectives on fat. Acta Physiol Scand. 2005;184:285–93.

    Article  Google Scholar 

  79. van Noordwijk MA, van Schaik CP. The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates. 1999;40(1):105–30.

    Article  PubMed  Google Scholar 

  80. van Schaik CP, van Noordwijk MA, Nunn CL. Sex and social evolution in primates. In: Lee PC, editor. Comparative Primate Socioecology. Cambridge: Cambridge University Press; 1999. p. 204–40.

    Chapter  Google Scholar 

  81. van Schaik CP, Isler K, Burkart JM. Explaining brain size variation: from social brain to cultural brain. Trends Cogn Sci. 2012;16(5):277–85.

    Article  PubMed  Google Scholar 

  82. van Woerden JT, van Schaik CP, Isler K. Effects of seasonality on brain size evolution: evidence from strepsirrhine primates. Am Nat. 2010;176(6):758–67.

    Article  PubMed  Google Scholar 

  83. van Woerden JT, Willems EP, van Schaik CP, Isler K. Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution. 2012;66:191–9.

    Article  PubMed  Google Scholar 

  84. Wells JCK. The Evolutionary Biology of Human Body Fatness. Cambridge: Cambridge University Press; 2010.

    Google Scholar 

  85. Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schurmann C, van Schaik CP. Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol. 2004;47(6):385–98.

    Article  CAS  PubMed  Google Scholar 

  86. Woodard HQ, White DR. The composition of body tissues. Br J Radiol. 1986;59:1209–19.

    Article  CAS  PubMed  Google Scholar 

  87. Wrangham R, Carmody R. Human adaptation to the control of fire. Evol Anthropol. 2010;19(5):187–99.

    Article  Google Scholar 

  88. Zihlman AL. Body build and tissue composition in Pan paniscus and Pan troglodytes, with comparisons to other hominoids. In: Susman RL, editor. The Pygmy Chimpanzee. New York: Plenum Press; 1984. p. 179–200.

    Chapter  Google Scholar 

  89. Zihlman AL, McFarland RK. Body mass in lowland gorillas: a quantitative analysis. Am J Phys Anthropol. 2000;113:61–78.

    Article  CAS  PubMed  Google Scholar 

  90. Zihlman AL, McFarland RK, Underwood CE. Functional anatomy and adaptation of male gorillas (Gorilla gorilla gorilla) with comparison to male orangutans (Pongo pygmaeus). Anat Rec. 2011;294(11):1842–55.

    Article  Google Scholar 

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Correspondence to Karin Isler Ph.D. .

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Isler, K. (2014). Adipose Tissue in Evolution. In: Fantuzzi, G., Braunschweig, C. (eds) Adipose Tissue and Adipokines in Health and Disease. Nutrition and Health. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-770-9_1

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  • DOI: https://doi.org/10.1007/978-1-62703-770-9_1

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