On the evolutionary origins of obesity: A new hypothesis

Endocrinology

Volumn 155, Issue 5, 2014, Pages 1573-1588

  Sellayah, Dyan ^a,b   Cagampang, Felino R ^c   Cox, Roger D ^a  

^a Genetics of Type 2 Diabetes Harwell Science and Innovation Campus ^*  (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ADRENERGIC RECEPTOR; MELANOCORTIN 4 RECEPTOR; UNCOUPLING PROTEIN 1;

AFRICA; BROWN ADIPOSE TISSUE; CLIMATE; DEVELOPED COUNTRY; DISEASE PREDISPOSITION; ENERGY EXPENDITURE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; ETHNIC DIFFERENCE; EVOLUTION; EVOLUTIONARY ADAPTATION; FAST FOOD; GAIN OF FUNCTION MUTATION; GENE FREQUENCY; GENETIC DRIFT; GENETIC SUSCEPTIBILITY; GENETIC TRAIT; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GEOGRAPHIC DISTRIBUTION; HUMAN; INDIGENOUS PEOPLE; INDUSTRIALIZATION; LIFESTYLE; METABOLIC RATE; METABOLIC SYNDROME X; NONHUMAN; OBESITY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW; THERMOREGULATION; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, BROWN; ANIMALS; BIOLOGICAL EVOLUTION; DEVELOPED COUNTRIES; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; METABOLIC SYNDROME X; MODELS, BIOLOGICAL; OBESITY; THERMOGENESIS;

EID: 84899418622     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-2103     Document Type: Review

References (200)

1. Kelly T, Yang W, Chen CS, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond). 2008; 32:1431-1437
2. Zaninotto P, Head J, Stamatakis E, Wardle H, Mindell J. Trends in obesity among adults in England from 1993 to 2004 by age and social class and projections of prevalence to 2012. J Epidemiol Community Health. 2009;63:140-146
3. Switzer NJ, Mangat HS, Karmali S. Current trends in obesity: body composition assessment, weight regulation, and emerging techniques in managing severe obesity. J Interv Gastroenterol. 2013; 3:34-36
4. Belardi V, Gallagher EJ, Novosyadlyy R, LeRoith D. Insulin and IGFs in obesity-related breast cancer. J Mammary Gland Biol Neoplasia. 2013;18:277-289
5. Rader DJ. Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the development of cardiovascular disease and diabetes mellitus. Am J Med. 2007;120(3 suppl 1):S12-S18
6. Smith SC Jr. Multiple risk factors for cardiovascular disease and diabetes mellitus. Am J Med. 2007;120(3 suppl 1):S3-S11
7. Labitigan M, Bahce-Altuntas A, Kremer JM, et al. Higher rates and clustering of abnormal lipids, obesity, and diabetes in psoriatic arthritis compared with rheumatoid arthritis [published online ahead of print October 7, 2013]. Arthritis Care Res. doi: 10.1002/ acr.22185
8. Zamosky L. The obesity epidemic. While America swallows $147 billion in obesity-related healthcare costs, physicians called on to confront the crisis. Med Econ. 2013;90:14-17
9. Aguilera CM, Olza J, Gil A. Genetic susceptibility to obesity and metabolic syndrome in childhood. Nutr Hosp. 2013;28(suppl 5): 44-55
10. Naukkarinen J, Rissanen A, Kaprio J, Pietilainen KH. Causes and consequences of obesity: The contribution of recent twin studies. Int J Obes (Lond). 2012;36:1017-1024
11. Nan C, Guo B, Warner C, et al. Heritability of body mass index in pre-adolescence, young adulthood and late adulthood. Eur J Epidemiol. 2012;27:247-253
12. Neel JV. Diabetes mellitus: A "thrifty" genotype rendered detrimental by "progress"? 1962. Bull World Health Organ. 1999;77: 694-703; discussion 692-693
13. Prentice AM, Rayco-Solon P, Moore SE. Insights from the developing world: Thrifty genotypes and thrifty phenotypes. Proc Nutr Soc. 2005;64:153-161
14. Song S. Assessing the impact of in utero exposure to famine on fecundity: Evidence from the 1959-61 famine in China. Popul Stud (Camb). 2013;67:293-308
15. Chakravarthy MV, Booth FW. Eating, exercise, and "thrifty" genotypes: connecting the dots toward an evolutionary understanding of modern chronic diseases. J Appl Physiol. 2004;96:3-10
16. Speakman JR. Thrifty genes for obesity, an attractive but flawed idea, and an alternative perspective: The 'drifty gene' hypothesis. Int J Obes (Lond). 2008;32:1611-1617
17. Speakman JR. A nonadaptive scenario explaining the genetic predisposition to obesity: The "predation release" hypothesis. Cell Metab. 2007;6:5-12
18. Speiser DI, Lampe RI, Lovdahl VR, Carrillo-Zazueta B, Rivera AS, Oakley TH. Evasion of predators contributes to the maintenance of male eyes in sexually dimorphic Euphilomedes ostracods (Crustacea). Integr Comp Biol. 2013;53:78-88
19. Spence R, Wootton RJ, Barber I, PrzybylskiM,Smith C. Ecological causes of morphological evolution in the three-spined stickleback. Ecol Evol. 2013;3:1717-1726
20. Lingle S, Feldman A, Boyce MS, Wilson WF. Prey behavior, agedependent vulnerability, and predation rates. Am Nat. 2008;172: 712-725
21. Quintana-Murci L, Semino O, Bandelt HJ, Passarino G, McElreavey K, Santachiara-Benerecetti AS. Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat Genet. 1999;23:437-441
22. Rasmussen M, Guo X, Wang Y, et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science. 2011; 334:94-98
23. Bowler JM, Johnston H, Olley JM, Prescott JR, Roberts RG, Shawcross W, Spooner NA. New ages for human occupation and climatic change at Lake Mungo, Australia. Nature. 2003;421:837-840
24. Emmelin A, FantahunM,Berhane Y, Wall S, Byass P. Vulnerability to episodes of extreme weather: Butajira, Ethiopia, 1998-1999. Glob Health Action. 2008;2
25. Haile M. Weather patterns, food security and humanitarian response in sub-Saharan Africa. Philos Trans R Soc Lond B Biol Sci. 2005;360:2169-2182
26. Slingo JM, Challinor AJ, Hoskins BJ, Wheeler TR. Introduction: food crops in a changing climate. Philos Trans R Soc Lond B Biol Sci. 2005;360:1983-1989
27. Scrimshaw NS. The phenomenon of famine. Annu Rev Nutr. 1987; 7:1-21
28. Hanson M, Gluckman P. Developmental origins of noncommunicable disease: population and public health implications.AmJ Clin Nutr. 2011;94(6 suppl):1754S-1758S
29. Hanson MA, Gluckman PD. Developmental origins of health and disease: Moving from biological concepts to interventions and policy. Int J Gynaecol Obstet. 2011;115(suppl 1):S3-S5
30. Voight BF, Kudaravalli S, Wen X, Pritchard JK. A map of recent positive selection in the human genome. PLoS Biol. 2006;4:e72
31. Kwiatkowski DP. How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 2005;77:171-192
32. Vuorisalo T, Arjamaa O, Vasemägi A, Taavitsainen JP, Tourunen A, Saloniemi I. High lactose tolerance in North Europeans: A result of migration, not in situ milk consumption. Perspect Biol Med. 2012;55:163-174
33. Atkins KE, Townsend JP, Medlock J, Galvani AP. Epidemiological mechanisms of genetic resistance to kuru. J R Soc Interface. 2013; 10:20130331
34. Nkenfou CN, Mekue LC, Nana CT, Kuiate JR. Distribution of CCR5-Delta32, CCR5 promoter 59029 A/G, CCR2-64I and SDF1-3′A genetic polymorphisms in HIV-1 infected and uninfected patients in the west region of Cameroon. BMC Res Notes. 2013;6:288
35. Schliekelman P, Garner C, Slatkin M. Natural selection and resistance to HIV. Nature. 2001;411:545-546
36. Hur SJ, Kim DH, Chun SC, Lee SK. Effect of adenovirus and influenza virus infection on obesity. Life Sci. 2013;93:531-535
37. Molofsky AB, Nussbaum JC, Liang HE, et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med. 2013;210:535-549
38. Winer DA, Winer S, Chng MH, Shen L, Engleman EG. B lymphocytes in obesity-related adipose tissue inflammation and insulin resistance. Cell Mol Life Sci. 2014;71:1033-1043
39. Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214
40. Hancock AM, Witonsky DB, Gordon AS, et al. Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet. 2008;4:e32
41. Albrecht SS, Gordon-Larsen P. Ethnic differences in body mass index trajectories from adolescence to adulthood: A focus on Hispanic and Asian subgroups in the United States. PLoS One. 2013; 8:e72983
42. Bryant AN, Ford KL, Kim G. Racial/ethnic variations in the relation between body mass index and cognitive function among older adults. Am J Geriatr Psychiatry [published online ahead of print October 11, 2013]. doi: 10.1016/j.jagp.2013.08.006
43. Caprio S, Daniels SR, Drewnowski A, et al. Influence of race, ethnicity, and culture on childhood obesity: Implications for prevention and treatment. Obesity (Silver Spring). 2008;16:2566-2577
44. Caprio S, Daniels SR, Drewnowski A, et al. Influence of race, ethnicity, and culture on childhood obesity: Implications for prevention and treatment: A consensus statement of Shaping America's Health and the Obesity Society. Diabetes Care. 2008;31:2211-2221
45. Kuzawa CW, Sweet E. Epigenetics and the embodiment of race: Developmental origins of US racial disparities in cardiovascular health. Am J Hum Biol. 2009;21:2-15
46. Zhang H, Rodriguez-Monguio R. Racial disparities in the risk of developing obesity-related diseases: A cross-sectional study. Ethn Dis. 2012;22:308-316
47. Kurian AK, Cardarelli KM. Racial and ethnic differences in cardiovascular disease risk factors: A systematic review. Ethn Dis. 2007;17:143-152
48. Crawford PB, Story M, Wang MC, Ritchie LD, Sabry ZI. Ethnic issues in the epidemiology of childhood obesity. Pediatr Clin North Am. 2001;48:855-878
49. Kumanyika SK. Obesity in minority populations: An epidemiologic assessment. Obes Res. 1994;2:166-182
50. Gordon-Larsen P, Adair LS, Popkin BM. The relationship of ethnicity, socioeconomic factors, and overweight in US adolescents. Obes Res. 2003;11:121-129
51. Finkelstein EA, Khavjou OA, Mobley LR, Haney DM, Will JC. Racial/ethnic disparities in coronary heart disease risk factors among WISEWOMAN enrollees. J Womens Health (Larchmt). 2004;13:503-518
52. Heald FP. Natural history and physiological basis of adolescent obesity. Fed Proc. 1966;25:1-3
53. Bray GA. Obesity: historical development of scientific and cultural ideas. Int J Obes. 1990;14:909-926
54. Swinburn BA, Caterson I, Seidell JC, James WP. Diet, nutrition and the prevention of excess weight gain and obesity. Public Health Nutr. 2004;7:123-146
55. Lichtenstein AH, Kennedy E, Barrier P, et al. Dietary fat consumption and health. Nutr Rev. 1998;56(5 Pt 2):S3-S19; discussion S19-S28
56. Rechel B, Mladovsky P, Ingleby D, Mackenbach JP, McKee M. Migration and health in an increasingly diverse Europe. Lancet. 2013;381:1235-1245
57. Rafnsson SB, Bhopal RS. Migrant and ethnic health research: report on the European Public Health Association Conference 2007. Public Health. 2008;122:532-534
58. Maffla C. Health in the age of migration: Migration and health in the EU. Community Pract. 2008;81:32-35
59. Friis R, Yngve A, Persson V. Review of social epidemiologic research on migrants' health: findings, methodological cautions, and theoretical perspectives. Scand J Soc Med. 1998;26:173-180
60. Loue S, Bunce A. The assessment of immigration status in health research. Vital Health Stat 2. 1999;127:1-115
61. Castañeda H. "Over-foreignization" or "unused potential?" A critical review of migrant health in Germany and responses toward unauthorized migration. Soc Sci Med. 2012;74:830-838
62. Gagnon AJ, Zimbeck M, Zeitlin J, et al. Migration to western industrialised countries and perinatal health: A systematic review. Soc Sci Med. 2009;69:934-946
63. Gagnon AJ, McDermott S, Rigol-Chachamovich J, Bandyopadhyay M, Stray-Pedersen B, Stewart D. International migration and gestational diabetes mellitus: A systematic review of the literature and meta-analysis. Paediatr Perinat Epidemiol. 2011;25:575-592
64. Lassetter JH, Callister LC. The impact of migration on the health of voluntary migrants in western societies. J Transcult Nurs. 2009; 20:93-104
65. Steffen PR, Smith TB, Larson M, Butler L. Acculturation to Western society as a risk factor for high blood pressure: A meta-analytic review. Psychosom Med. 2006;68:386-397
66. Shrestha LB. The Changing Demographic Profile of the Unites States. Congressional Research Service Report to Congress. Washington, DC: Congressional Research Service; 2011
67. Taveras EM, Gillman MW, Kleinman KP, Rich-Edwards JW, Rifas-Shiman SL. Reducing racial/ethnic disparities in childhood obesity: The role of early life risk factors. JAMA Pediatr. 2013;167: 731-738
68. Maskarinec G, Grandinetti A, Matsuura G, et al. Diabetes prevalence and body mass index differ by ethnicity: The Multiethnic Cohort. Ethn Dis. 2009;19:49-55
69. Gatineau M, Mathrani S. Obesity and Ethnicity. National Obesity Observatory, Oxford, UK; 2011
70. Prentice AM, Hennig BJ, Fulford AJ. Evolutionary origins of the obesity epidemic: Natural selection of thrifty genes or genetic drift following predation release? Int J Obes (Lond). 2008;32:1607-1610
71. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA. 2002;288: 1723-1727
72. Singh GK, Siahpush M, Hiatt RA, Timsina LR. Dramatic increases in obesity and overweight prevalence and body mass index among ethnic-immigrant and social class groups in the United States, 1976-2008. J Community Health. 2011;36:94-110
73. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM. The epidemiology of obesity. Gastroenterology. 2007;132:2087-2102
74. Singh GK, Kogan MD, Yu SM. Disparities in obesity and overweight prevalence among US immigrant children and adolescents by generational status. J Community Health. 2009;34:271-281
75. WangY, BeydounMA.The obesity epidemic in the United States- gender, age, socioeconomic, racial/ethnic, and geographic characteristics: A systematic review and meta-regression analysis. Epidemiol Rev. 2007;29:6-28
76. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277-359
77. Stock MJ, Rothwell NJ. Factors influencing brown fat and the capacity for diet-induced thermogenesis. Int J Obes (Lond). 1985; 9(Suppl 2):9-15
78. Brooks SL, Rothwell NJ, Stock MJ, Goodbody AE, Trayhurn P. Increased proton conductance pathway in brown adipose tissue mitochondria of rats exhibiting diet-induced thermogenesis. Nature. 1980;286:274-276
79. Nicholls DG, Bernson VS, Heaton GM. The identification of the component in the inner membrane of brown adipose tissue mitochondria responsible for regulating energy dissipation. Experientia Suppl. 1978;32:89-93
80. Gilsanz V, Smith ML, Goodarzian F, Kim M, Wren TA, Hu HH. Changes in brown adipose tissue in boys and girls during childhood and puberty. J Pediatr. 2012;160:604-609.e601
81. Ponrartana S, Hu HH, Gilsanz V. On the relevance of brown adipose tissue in children. Ann NY Acad Sci. 2013;1302:24-29
82. Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue uncoupling protein content in human infants, children and adults. Clin Sci (Lond). 1986;71:291-297
83. Chen KY, Brychta RJ, Linderman JD, et al. Brown fat activation mediates cold-induced thermogenesis in adult humans in response to a mild decrease in ambient temperature. J Clin Endocrinol Metab. 2013;98:E1218-E1223
84. Hu HH, Tovar JP, Pavlova Z, Smith ML, Gilsanz V. Unequivocal identification of brown adipose tissue in a human infant. J Magn Reson Imaging. 2012;35:938-942
85. Friedman M. "Brown fat" as a source of heat production in the newborn. Midwife Health Visitor. 1967;3:75-76
86. Lutz L, Perlstein PH. Temperature control in newborn babies. Nurs Clin North Am. 1971;6:15-23
87. Hackman PS. Recognizing and understanding the cold-stressed term infant. Neonatal Netw. 2001;20:35-41
88. Mance MJ. Keeping infants warm: challenges of hypothermia. Adv Neonatal Care. 2008;8:6-12
89. Hanna JM.Humanheat tolerance: An anthropological perspective. Annu Rev Anthropol. 1983;12:259-284
90. Haldane JBS. The Causes of Evolution. Princeton, NJ: Princeton University Press; 1932
91. Zhivotovsky LA, Rosenberg NA, Feldman MW. Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. Am J Hum Genet. 2003;72:1171-1186
92. Armitage SJ, Jasim SA, Marks AE, Parker AG, Usik VI, Uerpmann HP. The southern route "out of Africa": Evidence for an early expansion of modern humans into Arabia. Science. 2011;331:453-456
93. Yuan CX, Ji Q, Meng QJ, Tabrum AR, Luo ZX. Earliest evolution of multituberculate mammals revealed by a new Jurassic fossil. Science. 2013;341:779-783
94. Luo ZX, Ji Q, Wible JR, Yuan CX. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science. 2003;302: 1934-1940
95. Ji Q, Luo ZX, Yuan CX, Wible JR, Zhang JP, Georgi JA. The earliest known eutherian mammal. Nature. 2002;416:816-822
96. Williams BA, Kay RF, Kirk EC. New perspectives on anthropoid origins. Proc Natl Acad Sci USA. 2010;107:4797-4804
97. Anderson BG, BellML.Weather-related mortality:howheat, cold, and heat waves affect mortality in the United States. Epidemiology. 2009;20:205-213
98. NewmanRW.Whyman is such a sweaty and thirsty naked animal: A speculative review. Hum Biol. 1970;42:12-27
99. Thomson ML.Acomparison between the number and distribution of functioning eccrine sweat glands in Europeans and Africans. J Physiol. 1954;123:225-233
100. Moskowitz DW. Hypertension, thermotolerance, and the "African gene": An hypothesis. Clin Exp Hypertens. 1996;18:1-19
101. Ruxton GD, Wilkinson DM. Avoidance of overheating and selection for both hair loss and bipedality in hominins. Proc Natl Acad Sci USA. 2011;108:20965-20969
102. Ruxton GD, Wilkinson DM. Thermoregulation and endurance running in extinct hominins: Wheeler's models revisited. J Hum Evol. 2011;61:169-175
103. Sharp TA, Bell ML, Grunwald GK, et al. Differences in resting metabolic rate between white and African-American young adults. Obes Res. 2002;10:726-732
104. Weyer C, Snitker S, Bogardus C, Ravussin E. Energy metabolism in African Americans: potential risk factors for obesity. Am J Clin Nutr. 1999;70:13-20
105. Melby CL, Ho RC, Jeckel K, Beal L, Goran M, Donahoo WT. Comparison of risk factors for obesity in young, nonobese African- American and Caucasian women. Int J Obes Relat Metab Disord. 2000;24:1514-1522
106. Foster GD, Wadden TA, Swain RM, Anderson DA, Vogt RA. Changes in resting energy expenditure after weight loss in obese African American and white women. Am J Clin Nutr. 1999;69: 13-17
107. Kimm SY, Glynn NW, Aston CE, et al. Racial differences in the relation between uncoupling protein genes and resting energy expenditure. Am J Clin Nutr. 2002;75:714-719
108. Cicarma E, Mørk C, Porojnicu AC, et al. Influence of narrowband UVB phototherapy on vitamin D and folate status. Exp Dermatol. 2010;19:e67-e72
109. Steegmann AT Jr, Platner WS. Experimental cold modification of cranio-facial morphology. Am J Phys Anthropol. 1968;28:17-30
110. So JK. Human biological adaptation to arctic and subarctic zones. Annu Rev Anthropol. 1980;9:63-82
111. Takasaki Y, Loy SF, Juergens HW. Ethnic differences in the relationship between bioelectrical impedance and body size. J Physiol Anthropol Appl Human Sci. 2003;22:233-235
112. Snodgrass JJ, Leonard WR, Sorensen MV, Tarskaia LA, Mosher MJ. The influence of basal metabolic rate on blood pressure among indigenous Siberians. Am J Phys Anthropol. 2008;137:145-155
113. Snodgrass JJ, Leonard WR, Tarskaia LA, Alekseev VP, Krivoshapkin VG. Basal metabolic rate in the Yakut (Sakha) of Siberia. Am J Hum Biol. 2005;17:155-172
114. Snodgrass JJ, Sorensen MV, Tarskaia LA, Leonard WR. Adaptive dimensions of health research among indigenous Siberians. Am J Hum Biol. 2007;19:165-180
115. Leonard WR, Sorensen MV, Galloway VA, et al. Climatic influences on basal metabolic rates among circumpolar populations. Am J Hum Biol. 2002;14:609-620
116. Milan FA, Evonuk E. Oxygen consumption and body temperatures of Eskimos during sleep. J Appl Physiol. 1967;22:565-567
117. Rode A, Shephard RJ. Basal metabolic rate of Inuit. Am J Hum Biol. 1995;7:723-729
118. Wong WW, Butte NF, Ellis KJ, et al. Pubertal African-American girls expend less energy at rest and during physical activity than Caucasian girls. J Clin Endocrinol Metab. 1999;84:906-911
119. Júlíusson PB, Roelants M, Eide GE, Hauspie R, Waaler PE, Bjerknes R. Overweight and obesity in Norwegian children: Secular trends in weight-for-height and skinfolds. Acta Paediatr. 2007;96:1333-1337
120. Midthjell K, Lee CM, Langhammer A, et al. Trends in overweight and obesity over 22 years in a large adult population: The HUNT Study, Norway. Clin Obes. 2013;3:12-20
121. Lin M, Chu CC, Lee HL, et al. Heterogeneity of Taiwan's indigenous population: possible relation to prehistoric Mongoloid dispersals. Tissue Antigens. 2000;55:1-9
122. Beals KL. Head form and climatic stress. Am J Phys Anthropol. 1972;37:85-92
123. Raghavan M, Skoglund P, Graf KE, et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature. 2014;505:87-91
124. Criado JR, Gilder DA, Kalafut MA, Ehlers CL. Obesity in American Indian and Mexican American men and women: Associations with blood pressure and cardiovascular autonomic control. Cardiovasc Psychiatry Neurol. 2013;2013:680687
125. Fontvieille AM, Lillioja S, Ferraro RT, Schulz LO, Rising R, Ravussin E. Twenty-four-hour energy expenditure in Pima Indians with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1992;35:753-759
126. Ravussin E, Bogardus C. Energy balance and weight regulation: genetics versus environment. Br J Nutr. 2000;83(suppl 1):S17-S20
127. Balaresque PL, Ballereau SJ, Jobling MA. Challenges in human genetic diversity: Demographic history and adaptation. Hum Mol Genet. 2007;16(Spec No 2):R134-R139
128. Rising R, Keys A, Ravussin E, Bogardus C. Concomitant interindividual variation in body temperature and metabolic rate. Am J Physiol. 1992;263(4 Pt 1):E730-E734
129. Spraul M, Ravussin E, Fontvieille AM, Rising R, Larson DE, Anderson EA. Reduced sympathetic nervous activity. A potential mechanism predisposing to body weight gain. J Clin Invest. 1993; 92:1730-1735
130. Young JH, Chang YP, Kim JD, et al. Differential susceptibility to hypertension is due to selection during the out-of-Africa expansion. PLoS Genet. 2005;1:e82
131. Amos W, Hoffman JI. Evidence that two main bottleneck events shaped modern human genetic diversity. Proc Biol Sci. 2010;277: 131-137
132. TammE, Kivisild T, ReidlaM,et al. Beringian standstill and spread of Native American founders. PLoS One. 2007;2:e829
133. Horai S, Kondo R, Nakagawa-Hattori Y, Hayashi S, Sonoda S, Tajima K. Peopling of the Americas, founded by four major lineages of mitochondrial DNA. Mol Biol Evol. 1993;10:23-47
134. Pritchard JK, Pickrell JK, Coop G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol. 2010;20:R208-R215
135. BodnerM,Perego UA, Huber G, et al. Rapid coastal spread of First Americans: Novel insights from South America's Southern Cone mitochondrial genomes. Genome Res. 2012;22:811-820
136. Darwin CR. The Voyage of the Beagle. Vol 29. New York, NY: PF Collier; 1909
137. Fisher FR. Man Living in the Arctic; Proceedings of a Conference, Quartermaster Research and Engineering Center, Natick, Massachusetts, 1, 2 December 1960. Washington, DC: The National Academies Press; 1961
138. Yesner DR. Prehistoric maritime adaptations of the subarctic and subantarctic zones: The Aleutian/Fuegian connection reconsidered. Arctic Anthropol. 2004;41:76-97
139. Cameron TC, O'Sullivan D, Reynolds A, Piertney SB, Benton TG. Eco-evolutionary dynamics in response to selection on life-history. Ecol Lett. 2013;16:754-763
140. González Burchard E, Borrell LN, Choudhry S, et al. Latino populations: A unique opportunity for the study of race, genetics, and social environment in epidemiological research. Am J Public Health. 2005;95:2161-2168
141. Wyndham CH, McPherson RK, Munro A. Reactions to heat of Aborigines and Caucasians. J Appl Physiol. 1964;19:1055-1058
142. Bakker LEH, Boon MR, van der Linden RAD, et al. Brown adipose tissue volume in healthy lean south Asian adults compared with white Caucasians: A prospective, case-controlled observational study. Lancet Diabetes Endocrinol [published online ahead of print November 12, 2013]. doi:10.1016/S2213-8587(13) 70156-6
143. Li M, McCulloch B, McDermott R. Metabolic syndrome and incident coronary heart disease in Australian indigenous populations. Obesity (Silver Spring). 2012;20:1308-1312
144. O'Dea K. Westernisation, insulin resistance and diabetes in Australian aborigines. Med J Aust. 1991;155:258-264
145. Davis J, Busch J, Hammatt Z, et al. The relationship between ethnicity and obesity in Asian and Pacific Islander populations: A literature review. Ethn Dis. 2004;14:111-118
146. Esperat MC, Inouye J, Gonzalez EW, Owen DC, Feng D. Health disparities among Asian Americans and Pacific Islanders. Annu Rev Nurs Res. 2004;22:135-159
147. Friedlaender JS, Friedlaender FR, Reed FA, et al. The genetic structure of Pacific Islanders. PLoS Genet. 2008;4:e19
148. Lee JY, Wakabayashi H, Wijayanto T, Hashiguchi N, Saat M, Tochihara Y. Ethnic differences in thermoregulatory responses during resting, passive and active heating: Application of Werner's adaptation model. Eur J Appl Physiol. 2011;111:2895-2905
149. Saat M, Tochihara Y, Hashiguchi N, Sirisinghe RG, Fujita M, Chou CM. Effects of exercise in the heat on thermoregulation of Japanese and Malaysian males. J Physiol Anthropol Appl Human Sci. 2005;24:267-275
150. Wildman RP, Gu D, Muntner P, et al. Trends in overweight and obesity in Chinese adults: between 1991 and 1999-2000. Obesity (Silver Spring). 2008;16:1448-1453
151. Levi JV, Vintner S, Richardson L, St Laurent R, Segal LM. F As in Fat: How Obesity Policies Are Failing in America. Washington, DC: Trust for America's Health; 2008
152. Ravussin E, Valencia ME, Esparza J, Bennett PH, Schulz LO. Effects of a traditional lifestyle on obesity in Pima Indians. Diabetes Care. 1994;17:1067-1074
153. Hancock AM, Clark VJ, Qian Y, Di Rienzo A. Population genetic analysis of the uncoupling proteins supports a role for UCP3 in human cold resistance. Mol Biol Evol. 2011;28:601-614
154. de Souza BM, Brondani LA, Boucas AP, et al. Associations between UCP1-3826A/G, UCP2-866G/A, Ala55Val and Ins/Del, and UCP3-55C/T polymorphisms and susceptibility to type 2 diabetes mellitus: case-control study and meta-analysis.PLoSOne. 2013;8:e54259
155. Oelkrug R, Goetze N, Exner C, et al. Brown fat in a protoendothermic mammal fuels eutherian evolution. Nat Commun. 2013; 4:2140
156. Saito S, Saito CT, Shingai R. Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene. 2008;408: 37-44
157. Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature. 2000;404:652-660
158. Au-Yong IT, Thorn N, Ganatra R, Perkins AC, Symonds ME. Brown adipose tissue and seasonal variation in humans. Diabetes. 2009;58:2583-2587
159. Stock MJ, Rothwell NJ. The role of brown fat in diet-induced thermogenesis. Int J Vitam Nutr Res. 1986;56:205-210
160. Rothwell NJ, Stock MJ. A role for brown adipose tissue in dietinduced thermogenesis. Nature. 1979;281:31-35
161. Ouellet V, Labb SM, Blondin DP, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545-552
162. Lowell BB, Bachman ES. ß-Adrenergic receptors, diet-induced thermogenesis, and obesity. J Biol Chem. 2003;278:29385-29388
163. Nielsen B. Does diet-induced thermogenesis change the preferred ambient temperature of humans? Eur J Appl Physiol Occup Physiol. 1987;56:474-478
164. Lanzola E, Tagliabue A, Bozzi G, Meroni G. Obesity, diet and body temperature. Ann Nutr Metab. 1991;35:274-283
165. Jia JJ, Tian YB, Cao ZH, et al. The polymorphisms of UCP1 genes associated with fat metabolism, obesity and diabetes. Mol Biol Rep. 2010;37:1513-1522
166. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203-209
167. Yoneshiro T, Ogawa T, Okamoto N, et al. Impact of UCP1 and beta3AR gene polymorphisms on age-related changes in brown adipose tissue and adiposity in humans. Int J Obes (Lond). 2013; 37:993-998
168. Nakayama K, Miyashita H, Yanagisawa Y, Iwamoto S. Seasonal effects of UCP1 gene polymorphism on visceral fat accumulation in Japanese adults. PLoS One. 2013;8:e74720
169. Forga L, Corbalán M, Marti A, Fuentes C, Martinez-Gonzalez MA, Martinez A. Influence of the polymorphism 03826 A3G in the UCP1 gene on the components of metabolic syndrome. An Sist Sanit Navar. 2003;26:231-236
170. Valve R, Heikkinen S, Rissanen A, Laakso M, Uusitupa M. Synergistic effect of polymorphisms in uncoupling protein 1 and ß3- adrenergic receptor genes on basal metabolic rate in obese Finns. Diabetologia. 1998;41:357-361
171. Dhall M, ChaturvediMM,Rai U, Kapoor S. Sex-dependent effects of the UCP1-3826 A/G polymorphism on obesity and blood pressure. Ethn Dis. 2012;22:181-184
172. Proenza AM, Poissonnet CM, Ozata M, et al. Association of sets of alleles of genes encodingß3-adrenoreceptor, uncoupling protein 1 and lipoprotein lipase with increased risk of metabolic complications in obesity. Int J Obes Relat Metab Disord. 2000;24:93-100
173. Matsushita H, Kurabayashi T, Tomita M, Kato N, Tanaka K. Effects of uncoupling protein 1 and beta3-adrenergic receptor gene polymorphisms on body size and serum lipid concentrations in Japanese women. Maturitas. 2003;45:39-45
174. Orava J, Nuutila P, Noponen T, et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring) [published online ahead of print April 2, 2013]. doi: 10.1002/oby.20456
175. Church C, Moir L, McMurray F, et al. Overexpression of Fto leads to increased food intake and results in obesity. Nat Genet. 2010; 42:1086-1092
176. Speliotes EK, Willer CJ, Berndt SI, et al. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet. 2010;42:937-948
177. Thorleifsson G, Walters GB, Gudbjartsson DF, et al. Genomewide association yields new sequence variants at seven loci that associate with measures of obesity. Nat Genet. 2009;41:18-24
178. Willer CJ, Speliotes EK, Loos RJ, et al. Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nat Genet. 2009;41:25-34
179. Fesinmeyer MD, North KE, Ritchie MD, et al. Genetic risk factors for BMI and obesity in an ethnically diverse population: results from the population architecture using genomics and epidemiology (PAGE) study. Obesity (Silver Spring). 2013;21:835-846
180. Godfrey KM, Sheppard A, Gluckman PD, et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes. 2011;60:1528-1534
181. Gurrieri F, AccadiaM.Genetic imprinting: The paradigm of Prader- Willi and Angelman syndromes. Endocr Dev. 2009;14:20-28
182. Shore A, Karamitri A, Kemp P, Speakman JR, Lomax MA. Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia. 2010;53:1164-1173
183. Kiskinis E, Hallberg M, Christian M, et al. RIP140 directs histone and DNA methylation to silence Ucp1 expression in white adipocytes. EMBO J. 2007;26:4831-4840
184. Wang H, Zhang Y, Yehuda-Shnaidman E, et al. Liver X receptor alpha is a transcriptional repressor of the uncoupling protein 1 gene and the brown fat phenotype. Mol Cell Biol. 2008;28:2187-2200
185. TaoYX.The melanocortin-4 receptor: physiology, pharmacology, and pathophysiology. Endocr Rev. 2010;31:506-543
186. Xi B, Chandak GR, Shen Y, Wang Q, Zhou D. Association between common polymorphism near the MC4R gene and obesity risk: A systematic review and meta-analysis. PLoS One. 2012;7: E45731
187. Xi B, Takeuchi F, Chandak GR, et al. Common polymorphism near the MC4R gene is associated with type 2 diabetes: Data from a meta-analysis of 123,373 individuals. Diabetologia. 2012;55: 2660-2666
188. Tataranni PA, Christin L, Snitker S, Paolisso G, Ravussin E. Pima Indian males have lower beta-adrenergic sensitivity than Caucasian males. J Clin Endocrinol Metab. 1998;83:1260-1263
189. Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518-1525
190. Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360:1509-1517
191. Johnson F, Mavrogianni A, Ucci M, Vidal-Puig A, Wardle J. Could increased time spent in a thermal comfort zone contribute to population increases in obesity? Obes Rev. 2011;12:543-551
192. Chechi K, Nedergaard J, Richard D. Brown adipose tissue as an anti-obesity tissue in humans. Obes Rev. 2014;15:92-106
193. Whittle A, Relat-Pardo J, Vidal-Puig A. Pharmacological strategies for targeting BAT thermogenesis. Trends Pharmacol Sci. 2013;34: 347-355
194. Shabalina IG, Petrovic N, de Jong JM, Kalinovich AV, Cannon B, Nedergaard J. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 2013;5:1196-1203
195. GiraltM,Villarroya F. White, brown, beige/brite: Different adipose cells for different functions? Endocrinology. 2013;154:2992-3000
196. Carobbio S, Rosen B, Vidal-Puig A. Adipogenesis: New insights into brown adipose tissue differentiation. J Mol Endocrinol. 2013; 51:T75-T85
197. Villarroya F, Vidal-Puig A. Beyond the sympathetic tone: The new brown fat activators. Cell Metab. 2013;17:638-643
198. Berg M, Ejnell H, Kovács A, et al. Replacement of a tracheal stenosis with a tissue-engineered human trachea using autologous stem cells: A case report. Tissue Eng Part A. 2014;20:389-397
199. Liu X, Zheng Z, Zhu X, et al. Brown adipose tissue transplantation improves whole-body energy metabolism. Cell Res. 2013;23:851-854
200. Stanford KI, Middelbeek RJ, Townsend KL, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123:215-223