Cited by 114Birth, Development, and HealthEvolutionary Psychology and Human BehaviorDiabetes, Cardiovascular Risks, and Lipoproteins

Evolutionary origins of insulin resistance: a behavioral switch hypothesis

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Watve, Milind G, Yajnik, Chittaranjan S·2007·BMC Evolutionary Biology

Abstract

BACKGROUND: Insulin resistance, which can lead to a number of diseases including type 2 diabetes and coronary heart disease, is believed to have evolved as an adaptation to periodic starvation. The "thrifty gene" and "thrifty phenotype" hypotheses constitute the dominant paradigm for over four decades. With an increasing understanding of the diverse effects of impairment of the insulin signaling pathway, the existing hypotheses are proving inadequate. PRESENTATION OF THE HYPOTHESIS: We propose a hypothesis that insulin resistance is a socio-ecological adaptation that mediates two phenotypic transitions, (i) a transition in reproductive strategy from "r" (large number of offspring with little investment in each) to "K" (smaller number of offspring with more investment in each) and (ii) a transition from "stronger to smarter" or "soldier to diplomat" i.e. from relatively more muscle dependent to brain dependent lifestyle. A common switch could have evolved for the two transitions since the appropriate environmental conditions for the two transitions are highly overlapping and interacting. TESTING THE HYPOTHESIS: Gestational insulin resistance diverts more energy through the placenta, resulting in increased investment per offspring. On the other hand, insulin resistance is associated with reduced ovulation. The insulin signaling pathway is also related to longevity. Insulin resistance diverts more nutrients to the brain as compared to muscle. Also, hyperinsulinemia has direct positive effects on cognitive functions of the brain. The hypothesis gets support from known patterns in human clinical data and recent research on the molecular interactions in the insulin signaling pathway. Further we state many predictions of the hypothesis that can be tested experimentally or epidemiologically. IMPLICATIONS OF THE HYPOTHESIS: The hypothesis can bring about a significant change in the line of treatment as well as public health policies for the control of metabolic syndrome.

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  • In evolutionary terms, women with a PCOS metabolic phenotype would have increased survival chances during times of environmental or physiological demand for altered energy metabolism, but be more vulnerable to the pathological effects of insulin resistance when exposed to modern lifestyle factors.

    “In evolutionary terms, women with a PCOS metabolic phenotype would have increased survival chances during times of environmental or physiological demand for altered energy metabolism, but be more vulnerable to the pathological effects of IR when exposed to modern lifestyle factors [14,17,159].”

    From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [159]

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  • Insulin resistance may have evolved as a switch in reproductive and metabolic strategies, since development of IR can result in anovulation and reduced fertility, in addition to differential energy repartitioning to specific tissues.

    “It has been proposed that IR may have evolved as a switch in reproductive and metabolic strategies, since the development of IR can result in anovulation and reduced fertility, in addition to differential energy repartitioning to specific tissues [159].”
  • Being able to vary the sensitivity and physiological action of insulin is thought to have conferred a significant adaptive survival role in many animals throughout evolutionary history.

    “Nevertheless, being able to vary the sensitivity and physiological action of insulin is thought to have conferred a significant adaptive survival role in many animals throughout evolutionary history [146,159].”

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  1. Reaven GM Muscle insulin resistance is the ("not so") thrifty genotype Diabetologia 1998 41 482 484 9562354 10.1007/s001250050933 · DOI
  2. Torres SH Obesity, insulin resistance and skeletal muscle characteristics Acta Cient Venz 1999 50 34 41 10513036
  3. Schwartz MW Porte D Jr Diabetes, obesity and the brain Science 2005 307 375 379 15662002 10.1126/science.1104344 · DOI · Paper page
  4. Neel JV Diabetes mellitus: a thrifty genotype rendered detrimental by progress? Am J Human Genet 1962 14 353 362 13937884 PMC1932342
  5. Ozanne SE Hales CN Thrifty yes, genetic no Diabetologia 1998 41 485 487 9562355 10.1007/s001250050934 · DOI
  6. Hales CN Barker DJ Clark PM Cox LJ Fall C Osmond C Winter PD Fetal and infant growth and impaired glucose tolerance at age 64 Br Med J 1991 303 1019 1022 1954451 PMC1671766
  7. McKeigue PM Shah B Marmot MG Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asians Lancet 1991 339 382 386 1671422 10.1016/0140-6736(91)91164-P · DOI · Paper page
  8. Phillips DI Hirst S Clark PM Hales CN Osmond C Fetal growth and insulin secretion in adult life Diabetologica 1994 37 592 596 7926344
  9. Stein CE Fall CH Kumaran K Osmond C Cox V Barker DJ Fetal growth and coronary heart disease in South India Lancet 1996 348 1269 1273 8909379 10.1016/S0140-6736(96)04547-3 · DOI
  10. Barker DJP Clark PM Fetal under-nutrition and disease in later life Rev Reprod 1997 2 105 112 9414472 10.1530/ror.0.0020105 · DOI
  11. Yajnik C Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult onset disease Proc Nutritional Soc 2000 59 257 265 10946794
  12. Eriksson JG Forsen T Tuomilehto J Osmond C Barker DJ Early growth and coronary heart disease in later life: longitudinal study Br Med J 2001 322 949 953 11312225 10.1136/bmj.322.7292.949 PMC31033 · DOI
  13. Potau N Gussinye M Sanchez Ufarte C Rique S Vicens-Calvet E Carrascosa A Hyperinsulinemia in pre- and post-pubertal children born small for gestation age Horm Res 2001 56 146 150 11910199 10.1159/000048110 · DOI
  14. Lazar MA How obesity causes diabetes: not a tall tale Science 2005 307 373 375 15662001 10.1126/science.1104342 · DOI
  15. Swinburn BA Nyomba BL Saad MF Zurlo F Raz I Knowler WC Insulin resistance associated with lower rates of body weight gain in Pima Indians J Clin Invest 1991 88 168 173 2056116 PMC296017
  16. Swinburn BA The thrifty genotype hypothesis: How does it look after 30 years? Diabet Med 1996 13 695 699 8862942 10.1002/(SICI)1096-9136(199608)13:8<695::AID-DIA170>3.0.CO;2-# · DOI
  17. Kloting N Bluher M Extended longevity and insulin signaling in adipose tissue Exp Gerontol 2005 40 878 883 16125891 10.1016/j.exger.2005.07.004 · DOI
  18. Unger RH Klotho-induced insulin resistance: a blessing in disguise? Nature Medicine 2006 12 56 57 16397569 10.1038/nm0106-56 · DOI
  19. Kahn BB Flier JS Obesity and insulin resistance J Clin Invest 2000 106 473 481 10953022 PMC380258
  20. Steppan CM Bailey ST Bhat S Brown EJ Banerjee RR Wright CM Patel HR Ahima RS Lazar MA The hormone resistin links obesity to diabetes Nature 2001 409 307 312 11201732 10.1038/35053000 · DOI · Paper page
  21. Barzilai N She L Liu BQ Vuguin P Cohen P Wang J Rossetti L Surgical removal of visceral fat reverses hepatic insulin resistance Diabetes 1999 48 94 98 9892227 10.2337/diabetes.48.1.94 · DOI
  22. Tuomilehto J Lindstrom J The major diabetes prevention trials Curr Diab Rep 2003 3 115 122 12728637
  23. Silventoinen K Sans S Tolonen H Monterde D Kuulasmaa K Kasteloot H Tuomilehto J Trends in obesity and energy supply in the WHO MONICA project Int J Obes Relat Metab Disord 2004 28 710 718 15007395 10.1038/sj.ijo.0802614 · DOI · Paper page
  24. Kensara OA Wooton SA Phillips DIW Patel M Hoffman DJ Jackson AA Elia M the Hertfordshire Study Group Substrate-energy metabolism and metabolic risk factors for cardiovascular disease in relation to fetal growth and adult body composition Am J Physiol Endocrinol Metab 2006 291 365 371 10.1152/ajpendo.00599.2005 16531506 · DOI
  25. Eriksson J Forsen T Tuomilehto J Osmond C Barker D Size at birth, fat-free mass and resting metabolic rate in adult life Horm Metab Res 2002 34 72 76 11972290
  26. Beck-Nielsen H General characteristics of the insulin resistance syndrome: prevalence and heritability. European group for the study of insulin resistance (EGIR) Drugs 1999 58 7 10 10576517 10.2165/00003495-199958001-00003 · DOI
  27. Vilbergsson S Sigurdsson G Sigvaldason H Hreidarsson AB Sigfusson N Prevalence and incidence of NIDDM in iceland: evidence for stable incidence among males and females 1967–1991- the Reykjavik study Diabet Med 1997 14 491 498 9212317 10.1002/(SICI)1096-9136(199706)14:6<491::AID-DIA365>3.0.CO;2-1 · DOI
  28. Mouratoff GJ Carroll NV Scott EM Diabetes Mellitus in Eskimos J Am Med Asso 2001 19 107 112 6071412
  29. Yudkin JS Non-insulin-dependent diabetes mellitus (NIDDM) in Asians in the UK Diabet Med 1996 13 S16 S18 8894475 10.1002/(SICI)1096-9136(199604)13:4<390::AID-DIA121>3.0.CO;2-4 · DOI
  30. Hara H Egusa G Yamakido M Incidence of non-insulin-dependent diabetes mellitus and its risk factors in Japanese-Americans living in Hawaii and Los Angeles Diabet Med 1996 13 S133 S142 8894497 10.1002/(SICI)1096-9136(199602)13:2<133::AID-DIA7>3.0.CO;2-2 · DOI
  31. Vaz M Ukyab TT Padmavathi R Kuriyan R Muthayyan Diffey B Kurpad AV Body fat topography in Indian and Tibetan males of low and normal body mass index Indian J Physiol Pharmocol 1999 42 179 185 10365309
  32. Zargar AH Khan AK Masoodi SR Laway BA Wani AI Bashir MI Dar FA Prevalence of type 2 diabetes mellitus and impaired glucose tolerance in the Kashmir valley of the Indian subcontinent Diab Res Clin Practice 2000 47 135 146 10.1016/S0168-8227(99)00110-2 10670914 · DOI
  33. O'Rahilly S Farooqi IS Genetics of obesity Phil Trans R Soc B 2006 361 1095 1105 16815794 10.1098/rstb.2006.1850 PMC1642700 · DOI
  34. Novak CM Kotz CM Levine JA Central orexin sensitivity, physical activity and obesity in diet-induced obese and diet-resistant rats Am J Physiol Endocrinol Metab 2005 290 E396 E403 16188908 10.1152/ajpendo.00293.2005 · DOI
  35. Holmang A Bjorntorp P The effects of testosterone on insulin sensitivity in male rats Acta Physiol Scand 1992 146 505 510 1492567
  36. Xu XF De Pergola G Bjorntorp P Testosterone increases lipolysis and the number of beta-adrenoceptors in male rat adipocytes Endocrinology 1991 128 379 382 1846106
  37. MacArthur RH Wilson EO Theory of Island Biogeography 1967 Princeton: Princeton University Press
  38. Pianka ER On r- and K- selection Am Nat 1970 104 592 597 10.1086/282697 · DOI
  39. Sinervo B Svensson E Comendant T Density cycles and an offspring quantity and quality game driven by natural selection Nature 2000 406 985 988 10984050 10.1038/35023149 · DOI
  40. Chisholm JS Burbank VK Evolution and inequality Int J Epidemiol 2001 30 206 211 11369714 10.1093/ije/30.2.206 · DOI
  41. Kehl RJ Krew MA Thomas A Catalano PM Fetal growth and body composition in Infants of women with diabetes mellitus during pregnancy J Maternal-Fetal Med 1996 5 273 280 10.1002/(SICI)1520-6661(199609/10)5:5<273::AID-MFM5>3.0.CO;2-E 8930799 · DOI
  42. Catalano PM Huston LP Thomas AJ Fung CM Effect of maternal metabolism of fetal growth and body composition Diab Care 1998 21 B85 B90 9704233
  43. Burgen GA Givens JR Kitabchi AE Correlation of hyperandrogenism with hyperinsulinaemia in polycystic ovarian disease J Clin Endocrinol Metab 1980 50 113 116 7350174
  44. Dunaif A Insulin resistance and the polycystic ovary syndrome: mechanism and implication for pathogenesis Endocrine Rev 1997 18 774 800 9408743 10.1210/er.18.6.774 · DOI
  45. O'Dale P Tanbo T Hang E Abyholm T The impact of insulin resistance on the outcome of ovulation induction with low-dose follicle stimulation hormone in women with polycystic ovary syndrome Hum Reprod 1998 13 567 570 9572412 10.1093/humrep/13.3.567 · DOI
  46. Homburg R The management of infertility associated with polycystic ovary syndrome Rep Biol Endocrinol 2003 1 109 10.1186/1477-7827-1-109 PMC280720 14617367 · DOI
  47. Huber-Buccholz MM Carey DG Norman RJ Potential by life style modification in obese polycystic ovary syndrome: role of insulin sensitivity and luteinizing hormone J Endocrinol Metab 1999 84 1470 1474 10.1210/jc.84.4.1470 10199797 · DOI · Paper page
  48. Greisen S Ledet T Ovesen P Effects of androstenedione, insulin and luteinizing hormone on steroidogenesis in human granulosa luteal cells Hum Reprod 2001 16 2061 2065 11574492 10.1093/humrep/16.10.2061 · DOI
  49. Saip Toprak Arif Yonem Bekir Cakir Serdar Guler Omer Azal Metin Ozata Ahmet Corakci Insulin Resistance in Nonobese Patients with Polycystic Ovary Syndrome Horm Res 2001 55 65 70 11509861
  50. Peters RH Ecological implications of body size 1983 Cambridge: Cambridge University Press
  51. Calder WA Size, function and life history 1984 Harvard University Press
  52. Kimura KD Tissenbaum HA Liu Y Ruvkun G daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans Science 1997 277 942 946 9252323 10.1126/science.277.5328.942 · DOI
  53. Bluher M Kahn BB Kahn CR Extended longevity in mice lacking the insulin receptor in adipose tissue Science 2003 299 572 574 12543978 10.1126/science.1078223 · DOI
  54. Zhang J Resveratrol inhibits insulin responses in a SirT1-independent pathway Biochem J 2006 397 519 527 16626303 10.1042/BJ20060044 PMC1533305 · DOI
  55. Bartke A Brown-Borg H Life extension in the dwarf mouse Curr Top Develop Biol 2004 63 189 225 15536017
  56. Cranston I Marsden P Matyka K Evans M Lomas J Sonksen P Maisey M Amiel SA Regional differences in cerebral blood flow and glucose utilization in diabetic man: the effect of insulin J of Cerebral Blood Flow & Metab 1998 18 130 140 10.1097/00004647-199802000-00002 9469154 · DOI
  57. Schubert M Gautam D Surjo D Ueki K Baudler S Schubert D Kondo T Alber J Galldiks N Kustermann E Arndt S Jacobs AH Krone W Kahn CR Bruning JC Role of neuronal insulin resistance in neurodegenerative diseases PNAS 2004 101 3100 3105 14981233 10.1073/pnas.0308724101 PMC365750 · DOI
  58. Zhao W-Q Alkon DL Role of insulin and insulin receptor in learning and memory Mol and Cell Endocrinol 2001 177 125 134 11377828 10.1016/S0303-7207(01)00455-5 · DOI
  59. Aizenman Y Weichsel ME Jean De Vellis Changes in insulin and transferrin requirements of pure brain neuronal cultures during embryonic development PNAS 1986 83 2263 2266 3515348 10.1073/pnas.83.7.2263 PMC323272 · DOI
  60. Lannert H Hoyer S Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats Behav Neurosci 1998 112 1199 1208 9829797 10.1037/0735-7044.112.5.1199 · DOI
  61. Farr SA Banks WA Morley JE Effects of leptin on memory processing Peptides 2006 27 1420 1425 16293343 10.1016/j.peptides.2005.10.006 · DOI
  62. Elias PK Elias MF D'Agostino RB Sullivan LM Wolf PA Serum cholesterol and cognitive performance in the Framingham heart study Psychosomatic Med 2005 67 24 30 10.1097/01.psy.0000151745.67285.c2 15673620 · DOI
  63. Arvanitakis Z Wilson RS Bienias JL Evans DA Bennett DA Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function Arch Neurol 2004 61 661 666 15148141 10.1001/archneur.61.5.661 · DOI · Paper page
  64. Rasgon N Jarvik L Insulin resistance, affective disorders, and alzheimer's disease: review and hypothesis J Gerontol 2004 59A 178 183 14999034
  65. Shiiki T Ohtsuki S Kurihara A Naganuma H Nishimura K Tachikawa M Hosoya K Terasaki T Brain insulin impairs Amyloid-β(1–40) clearance from the brain J Neurosci 2004 24 9632 9637 15509750 10.1523/JNEUROSCI.2236-04.2004 PMC6730166 · DOI
  66. Ryan CM Geckle M Why is learning and memory dysfunction in type 2 diabetes limited to older adults Diabetes Metab Res Rev 2000 16 308 315 11025555 10.1002/1520-7560(2000)9999:9999<::AID-DMRR141>3.0.CO;2-X · DOI
  67. Xie L Helmerhorst E Taddei K Plewright B van Bronswijk W Martins R Alzheimer's β-amyloid peptides compete for insulin binding to the insulin receptor J Neurosci 2002 22 RC221 RC226 12006603 PMC6757630
  68. Zhao L Teter B Morihara T Lim GP Ambegaokar SS Ubeda OJ Frautschy SA Cole GM Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention J Neurosci 2004 24 11120 11126 15590928 10.1523/JNEUROSCI.2860-04.2004 PMC6730264 · DOI · Paper page
  69. Craft S Peskind E Schwartz MW Schellenberg GD Raskind M Porter D Jr Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype Neurology 1998 50 164 168 9443474
  70. Craft S Asthana S Newcomer JW Wilkinson CW Matos IT Baker LD Cherrier M Lpfgreem C Latemdresse S Petrova A Plumate S Raskind M Grimwood K Veith RC Enhancement of memory in Alzheimer disease with insulin and somatostatin but not glucose Arch Gen Psychiatry 1999 56 1135 1140 10591291 10.1001/archpsyc.56.12.1135 · DOI · Paper page
  71. Freychet P Insulin receptors and insulin actions in the nervous system Diab Metab Res Rev 2000 16 390 392 10.1002/1520-7560(200011/12)16:6<390::AID-DMRR161>3.0.CO;2-T 11114099 · DOI
  72. Kern W Peters A Fruehwald-Schultes B Deininger E Born J Fehm HL Improving influence of insulin on cognitive functions in humans Neuroendocrinology 2001 74 270 280 11598383 10.1159/000054694 · DOI · Paper page
  73. Zimmet P Dowse G Finch C The epidemiology and natural history of NIDDM- lessons from south pacific Diab Metab Rev 1990 6 91 112 2198152
  74. Mbanya JCN Ngogang J Salah JN Minhoulou E Balkau B Prevalence of NIDDM and impaired glucose tolerance in a rural and urban population in Cameroon Diabetologia 1997 40 824 829 9243104 10.1007/s001250050755 · DOI
  75. Zhao W Chen H Xu H Moore E Meiri N Quon M Alkon D Brain insulin receptors and spatial memory J Biol Chem 1999 274 34893 34902 10574963 10.1074/jbc.274.49.34893 · DOI
  76. Fruehwald-Schultes B Peters A Born J Fehm HL Kern W Adaptation of cognitive function to hypoglycemia in healthy men Diab Care 2000 23 1059 1066 10.2337/diacare.23.8.1059 10937498 · DOI
  77. Winick M Rosso P Waterlow JC Cellular growth of cerebrum, cerebellum and brain stem in normal and merasmic children Exp Neurol 1970 26 393 400 5414374 10.1016/0014-4886(70)90134-2 · DOI
  78. Winick M Malnutrition and brain development J Pediatr 1969 74 667 679 4888313 10.1016/S0022-3476(69)80129-0 · DOI
  79. Silventoinen K Posthume D Beijsterveldt T Bartels M Boomsma DI Genetic contributions to the association between height and intelligence: evidence from Dutch twin data from childhood to middle age Genes Brain Behav 2006 5 585 595 17081263 10.1111/j.1601-183X.2006.00208.x · DOI
  80. Sade DS Altmann S Determinants of dominance in a group of free-ranging rhesus monkeys Social communication among primates 1967 Chicago: Chicago University Press 99 114
  81. Cheney DL The play partners of immature baboons Anim Behav 1978 26 1038 1050 10.1016/0003-3472(78)90093-3 · DOI
  82. Datta SB Hinde RA Relative power and the acquisition of rank Primate social relationships: An integrated approach 1983 Blackwell: Oxford University Press 93 103
  83. Chapais B Harcourt AH, de Waal FBM The role of alliances in social inheritance of rank among female primates Coalitions and alliances in humans and other primates 1992 Oxford: Oxford University Press 29 59
  84. Peters A Schweiger U Pellerin L Hubold C Oltmanns KM Conrad M Schultes B Born J Fehm HL The selfish brain: competition for energy resources Neurosc Behav Rev 2004 28 143 180 15172762
  85. Breiter JS Aharon I Kahneman D Dale A Shizal P Functional imaging of neural responses to expectancy and experience of monetary gains and losses Neuron 2001 30 619 639 11395019 10.1016/S0896-6273(01)00303-8 · DOI · Paper page
  86. Elliot R Newman JL Longe OA William Deakin JF Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: a parametric functional magnetic resonance imaging study J Neurosci 2003 23 303 307 12514228 PMC6742125
  87. Briers B Pandelaere M Dewitte S Warlop L Hungry for money: the desire for caloric resources increases the desire for financial resources and vice versa? Psychol Sci 2006 17 939 943 17176423 10.1111/j.1467-9280.2006.01808.x · DOI
  88. Reisbick S Neuringer M Hasnain R Connor WE Home Cage Behaviour of Rhesus Monkeys with Long-Term Deficiency of Omega-3 Fatty Acids Physiol Behav 1994 55 231 239 8153160 10.1016/0031-9384(94)90128-7 · DOI
  89. Hibbeln JR Salem N Jr Dietary polyunsaturated fatty acids and depression: when cholesterol does not satisfy Am J Clin Nutr 1995 62 1 9 7598049
  90. Stevens LJ Zenta SS ll Abate ML Kuczek T Burgess JR Omega-3 fatty acids in boys with behaviour, learning, and health problems Physiol Behav 1996 59 915 920 8778886 10.1016/0031-9384(95)02207-4 · DOI
  91. Hibbeln JR Umbau JC Linnoila M George DT Ragan PW Shoaf SE Vaughan MR Rawlings R Salem N Jr A replication study of violent and nonviolent subjects: cerebrospinal fluid metabolites of serotonin and dopamine are predicted by plasma essential fatty acids Biol Psychiatry 1998 44 243 249 9715355 10.1016/S0006-3223(98)00143-7 · DOI
  92. Willatts P Forsyth JS DiModugno MK Varma S Colvin M Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age Lancet 1998 352 688 691 9728984 10.1016/S0140-6736(97)11374-5 · DOI
  93. Zahavi A The Handicap Principle 1997 Oxford: Oxford University Press
  94. Braude S Tang-Martinez Z Taylor G Stress, testosterone and the immunoredistribution hypothesis Behav Ecol 1999 10 345 349 10.1093/beheco/10.3.345 · DOI
  95. Ridker PM Evaluating novel cardiovascular risk factors: Can we better predict heart attacks? Ann Int Med 1999 130 933 937 10375342
  96. Misra A Vikram NK Insulin resistance syndrome (metabolic syndrome) and Asian Indians Cur Sci 2002 83 1483 1496 //Nutrition 2004, 20(5):482–491
  97. Sjoholm A Nystrom R Endothelial inflammation in insulin resistance Lancet 365 610 612 15708106
  98. Festa A D'Agostino R Howard G Mykkanen L Tracey RP Haffner SM Chronic subclinical inflammation as part of the insulin resistance syndrome. The insulin resistance atherosclerosis study (IRAS) Circulation 2000 102 42 47 10880413
  99. Grimble RF Inflammatory status and insulin resistance Curr Opin Clinic Nut Metab Care 2002 5 551 559 10.1097/00075197-200209000-00015 12172480 · DOI
  100. Xu H Barnes GT Yang Q Tan G Yang D Chou CJ Sole J Nichols A Ross JS Tartaglia AA Chen H Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J Clin Invest 2003 112 1821 1830 14679177 10.1172/JCI200319451 PMC296998 · DOI · Paper page
  101. van Westerloo DJ Florquin S de Boer AM Daalhuisen J de Vos AF Bruno MJ van der Poll T Therapeutic effects of troglitazone in experimental chronic pancreatitis in mice Am J Pathol 2005 166 721 728 15743784 PMC1602356
  102. Xu X De Pergola G Bjorntorp P The effects of androgens on the regulation of lipolysis in adipose precursor cells Endocrinology 1990 126 1229 1234 2153523
  103. Rebuffe-Scrive M Marin P Bjorntorp P Effect of testosterone on abdominal adipose tissue in men Int J Obes 1991 15 791 795 1778664
  104. Khaw KT Barrett-Connor E Lower endogenous androgens predict central adiposity in men Am J Epidemiol 1992 2 675 682 1342319
  105. Marin P Holmang S Jonsson L Sjostrom L Kvist H Holm G Lindstedt G Bjorntorp P The effects of testosterone treatment on body composition and metabolism in middle-aged obese men Int J Obes Relat Metab Disord 1992 16 991 997 1335979
  106. Marin P Arver S Androgens and abdominal obesity Bailliers Clin Endocrinol Metab 1998 12 441 451 10.1016/S0950-351X(98)80191-2 10332565 · DOI
  107. Muller M Grobbee DE den Tonkelaar I Lamberts SW van der Schouw YT Endogenous sex hormones and metabolic syndrome in aging men J Clin Endocrinol Metab 2005 90 2618 2623 15687322 10.1210/jc.2004-1158 · DOI · Paper page
  108. Pitteloud N Mootha VK Dwyer AA Hardin M Lee H Eriksson K-F Tripathi D Yialamas M Groop L Elahi D Hayes FJ Relationship between testosterone levels, insulin sensitivity and mitochondrial function in men Diab Care 2005 28 1636 1642 10.2337/diacare.28.7.1636 15983313 · DOI · Paper page
  109. Shores MM Matsumoto AM Sloan KL Kivlahan DR Low serum testosterone and mortality in male veterans Arch Intern Med 2006 166 1660 1665 16908801 10.1001/archinte.166.15.1660 · DOI
  110. Kurosu H Yamamoto M Clark JD Pastor JV Nandi A Gurnani P McGuiness OP Chikuda H Yamaguchi M Kawaguchi HK Shimomura I Takayama Y Herz J Kahn R Rosenblatt KP Kuro-o M Suppression of aging in mice by the hormone klotho Science 2005 309 1829 1833 16123266 10.1126/science.1112766 PMC2536606 · DOI · Paper page
  111. Wang SL Pan WH Hwn CM Ho LT Lo CH Lin SL Jong YS Incidence of NIDDM and the effects of gender, obesity and hyperinsulinaemia in Taiwan Diabetologia 1997 40 1431 1438 9447951 10.1007/s001250050846 · DOI
  112. Ramchandran A Jali MV Mohan V Snehalatha C Viswanathan M High prevalence of diabetes in an urban population in South India Br Med J 1988 297 587 590 3139221 PMC1834545
  113. Mohan V Shanthirani S Deepa R Premalatha G Sastry NG Saroja R Intra-urban differences in the prevalence of the metabolic syndrome in southern India – the Chennai urban population study (CUPS No. 4) Diabet Med 2001 18 280 287 11437858 10.1046/j.1464-5491.2001.00421.x · DOI
  114. Hardikar A Role of environmental factors in induction, prevention, and reversal of diabetes mellitus PhD thesis 1999 University of Pune
  115. Russell-Jones DL Hoskins P Kearney E Morris R Katoaga S Slavin B Turtle JR Rural urban differences of diabetes – impaired glucose tolerance, hypertension, obesity, glycosolated haemoglobin, nutritional proteins, fasting cholesterol and apolipoproteins in Fijian Melanesians over 40 Quart J Med 1990 74 75 81 2109332
  116. Snehalatha C Ramachandran A Vijay V Vishwanatha M Differences in plasma insulin responses in urban and rural Indians: a study in southern Indians Diabet Med 1994 11 445 448 8088121
  117. Al-Nuaim AR Prevalence of glucose intolerance in urban and rural communities in Saudi Arabia Diabet Med 1997 14 595 602 9223399 10.1002/(SICI)1096-9136(199707)14:7<595::AID-DIA377>3.0.CO;2-C · DOI
  118. Harsha Rao R Diabetes in the undernourished: coincidence or consequence? Endocrine Rev 1988 9 67 87 3286236
  119. Chaturvedi N Jarrett J Shipley MJ Fuller JH Socioeconomic gradient in morbidity and mortality in people with diabetes: cohort study findings from the Whitehall study and the WHO multinational study of vascular disease in diabetes Br Med J 1998 316 100 105 9462313 PMC2665385
  120. Connolly V Unwin N Sherriff P Bilous R Kelly W Diabetes prevalence and socioeconomic status: a population based study showing increased prevalence of type 2 diabetes mellitus in deprived areas J Epidemiol Commun Health 2000 54 173 177 10.1136/jech.54.3.173 PMC1731634 10746110 · DOI
  121. Evans JM Newton RW Ruta DA MacDonald TM Morris AD Socio-economic status, obesity and prevalence of type 1 and type 2 diabetes mellitus Diabet Med 2000 178 478 10975218 10.1046/j.1464-5491.2000.00309.x · DOI
  122. Kumari Meena Head J Marmot M Prospective study of social and other risk factors for incidence of type 2 diabetes in the Whitehall II study Arch Intern Med 2004 164 1873 1880 15451762 10.1001/archinte.164.17.1873 · DOI
  123. Dalstra JA Kunst AE Borrell C Breeze E Cambois E Costa G Geurts JJ Lahelma E Van Oyen H Rasmussen NK Regidor E Spadea T Mackenbach JP Socioeconomic differences in the prevalence of common chronic diseases: an overview of eight European countries Int J Epidemiol 2005 34 316 326 15737978 10.1093/ije/dyh386 · DOI
  124. Alley DA Seeman TE Kim JK Karlamangla A Hu P Crimmins EM Socioeconomic status and c-reactive protein levels in the US population:NHANES IV Brain Behav Immunity 2006 20 498 504 10.1016/j.bbi.2005.10.003 16330181 · DOI
  125. Kington RS Smith JP Socioeconomic status and racial and ethnic differences in functional status associated with chronic diseases Am J Pub Health 1997 87 805 810 9184510 PMC1381054
  126. Robbins JM Vaccarino V Zhang H Kasl SV Excess type 2 diabetes in African-American women and men aged 40–74 and socioeconomic status: evidence from the third national health and nutrition examination survey J Epidemiol Commun Health 2000 54 839 845 10.1136/jech.54.11.839 PMC1731578 11027198 · DOI
  127. Stern MP Rosenthal M Haffner SM Hazuda HP Franco LJ Sex difference in the effects of sociocultural status on diabetes and cardiovascular risk factors in Mexican Americans – the San Antonio heart study Am J Epidemiol 1984 120 834 851 6507426
  128. Ramchandran A Snehalatha C Latha E Vijay V Viswanathan M Rising prevalence of NIDDM in an urban population in India Diabetologia 1997 40 232 237 9049486 10.1007/s001250050668 · DOI
  129. Riste L Khan F Cruickshank K High prevalence of type 2 diabetes in all ethnic groups including Europeans in a British inner city Diab Care 2001 24 1377 1383 10.2337/diacare.24.8.1377 11473073 · DOI
  130. Ellaway A Macintyre S Bonnefoy X Graffiti, greenery and obesity in adults: secondary analysis of European cross sectional survey Br Med J 2005 331 611 612 16113034 10.1136/bmj.38575.664549.F7 PMC1215553 · DOI
  131. Trivers RL Willard DE Natural selection of parental ability to vary the sex ratio of offspring Nature 1973 179 90 92 4682135

Authors
Watve, M. G., & Yajnik, C. S.
Affiliations
King Edward Memorial Hospital Research Centre (IN)
Corresponding author
Watve, Milind G
Venue
BMC Evolutionary Biology
Published
2007
Volume
7
Issue
1
Pages
61
ISSN
1471-2148 (ISSN-L)
OpenAlex
W2087275359
Cited by
114
References
156
Citations by year
2026: 4 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 5 · 2021: 4 · 2020: 8 · 2019: 7 · 2018: 3 · 2017: 5 · 2016: 5 · 2015: 9 · 2014: 6 · 2013: 6 · 2012: 11
FWCI
7.34
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Keywords
insulin resistance, evolutionary origin, thrifty gene hypothesis, thrifty phenotype, ovulation, longevity, hyperinsulinemia, cognitive function, metabolic syndrome, type 2 diabetes, coronary artery disease
MeSH terms
Adaptation, Physiological, Animals, Biological Evolution, Humans, Insulin Resistance, Phenotype, Reproduction, Selection, Genetic, Weight Gain, Metabolic Syndrome

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