Skip to main content
×
×
Home

Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins

  • Michael L. Power (a1) (a2) and Jay Schulkin (a1) (a3)
Abstract

Human beings are susceptible to sustained weight gain in the modern environment. Although both men and women can get fat, they get fat in different ways, and suffer different consequences. We review differences between men and women in the incidence of obesity, fat deposition patterns, fat metabolism, and the health consequences of obesity, and examine potential evolutionary explanations for these differences. Women generally have a larger proportion of body mass as fat, and are more likely to deposit fat subcutaneously and on their lower extremities; men are more likely to deposit fat in the abdominal region. Excess adipose tissue in the abdominal region, especially visceral fat, is associated with more health risks. Women have higher rates of reuptake of NEFA into adipose tissue; however, they also have higher rates of fat oxidation during prolonged exercise. Oestrogen appears to underlie many of these differences. Women bear higher nutrient costs during reproduction. Fat and fertility are linked in women, through leptin. Low leptin levels reduce fertility. Ovarian function of adult women is associated with their fatness at birth. In our evolutionary past food insecurity was a frequent occurrence. Women would have benefited from an increased ability to store fat in easily metabolisable depots. We suggest that the pattern of central obesity, more commonly seen in men, is not adaptive, but rather reflects the genetic drift hypothesis of human susceptibility to obesity. Female obesity, with excess adiposity in the lower extremities, reflects an exaggeration of an adaptation for female reproductive success.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Dr Michael L. Power, fax +1 202 554 4346, email mpower@ACOG.ORG
References
Hide All
1Committee on Youth Population and Military Recruitment: Physical, Medical, and Mental Health Standards, National Research Council (2006) Assessing Fitness for Military Enlistment: Physical, Medical, and Mental Health Standards [Sackett PR and Mavor AS, editors]. Washington, DC: The National Academies Press.
2Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR & Flegal KM (2004) Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA 291, 28472850.
3Moore TR (2004) Adolescent and adult obesity in women: a tidal wave just beginning. Clin Obstet Gynecol 47, 884889.
4Hebebrand J, Wulftange H, Goerg T, Ziegler A, Hinney A, Barth N, Mayer H & Remschmidt H (2000) Epidemic obesity: are genetic factors involved via increased rates of assortative mating? Int J Obesity 24, 345353.
5Woods SC, Gotoh K & Clegg DJ (2003) Gender differences in the control of energy homeostasis. Exp Biol Med 228, 11751180.
6Williams CM (2004) Lipid metabolism in women. Proc Nutr Soc 63, 153160.
7Mittendorfer B (2005) Sexual dimorphism in human lipid metabolism. J Nutr 135, 681686.
8Nielson S, Guo ZK, Johnson M, Hensrud DD & Jensen MD (2004) Splanchic lipolysis in human obesity. J Clin Invest 113, 15821588.
9Rodríguez G, Samper MP, Olivares JL, Ventura P, Moreno LA & Pérez-González JM (2005) Skinfold measurements at birth: sex and anthropometric influence. Arch Dis Child Fetal Neonatal Ed 90, F273F275.
10He Q, Horlick M, Thornton J, Wang J, Pierson RN Jr, Heshka S & Gallagher D (2004) Sex-specific fat distribution is not linear across pubertal groups in a multiethnic study. Obes Res 12, 725733.
11Lemieux S, Prud'homme D, Bouchard C, Tremblay A & Deprés J-P (1993) Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 58, 463467.
12Kuk JL, Lee SJ, Heymsfield SB & Ross R (2005) Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 81, 13301334.
13Arner P (1998) Not all fat is alike. Lancet 351, 13011302.
14Racette SB, Hagberg JM, Evans EM, Holloszy JO & Weiss EP (2006) Abdominal obesity is a stronger predictor of insulin resisitance than fitness among 50–95 year olds. Diabetes Care 29, 673678.
15Goodpaster BH, Krishnaswami S, Harris TB, Katsiaras A, Kritchevsky SB, Simonsick EM, Nevitt M, Holvoet P & Newman AB (2005) Obesity, regional body fat distribution, and the metabolic syndrome in older men and women. Arch Intern Med 165, 777783.
16Van Pelt RE, Evans EM, Schechtman KB, Ehsani AA & Kohrt WM (2002) Contributions of total and regional fat mass to risk for cardiovascular disease in older women. Am J Physiol Endocrinol Metab 282, E1023E1028.
17Karelis AD, St-Pierre DH, Conus F, Rabasa-Lhoret R & Poehlman ET (2004) Metabolic and body composition factors in subgroups of obesity: what do we know? J Clin Endocrinol Metab 89, 25692575.
18Garg A (2004) Regional adiposity and insulin resistance. J Clin Endocrinol Metab 89, 42064210.
19Jensen MD (2006) Is visceral fat involved in the pathogenesis of the metabolic syndrome? Human model. Obesity 14, Suppl., 20S24S.
20Fujioka S, Matsuzawa Y, Tokunaga K & Tarui S (1987) Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism 36, 5459.
21Seppälä-Lindroos A, Vehkavaara S, Hakkinen AM, Goto T, Westerbacka J, Sovijarvi A, Halavaara J & Yki-Jarvinen H (2002) Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 87, 30233028.
22Bergman RN, Kim SP, Catalano KJ, Hsu IR, Chiu JD, Kabir M, Hucking K & Ader M (2006) Why visceral fat is bad: mechanisms of the metabolic syndrome. Obesity 14, Suppl., 16S19S.
23Koutsari C & Jensen MD (2006) Free fatty acid metabolism in human obesity. J Lipid Res 47, 16431650.
24Jensen MD, Cryer PE, Johnson CM & Murray MJ (1996) Effects of epinephrine on regional free fatty acid and energy metabolism in men and women. Ann Rev Physiol 33, 259264.
25Pasquali R, Cantobelli S, Casimirri F, Capelli M, Bortoluzzi L, Flamia R, Labate AMM & Barbara L (1993) The hypothalamic-pituitary-adrenal axis in obese women with different patterns of body fat distribution. J Clin Endocrinol Metab 77, 341346.
26Deurenberg P, Deurenberg-Yap M & Guricci S (2002) Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev 3, 141146.
27Park Y-W, Allison DB, Heymsfield SB & Gallagher D (2001) Larger amounts of visceral adipose tissue in Asian Americans. Obes Res 9, 381387.
28Yajnik CS (2004) Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J Nutr 134, 205210.
29Conway JM, Yanovski SZ, Avila NA & Hubbard VS (1995) Visceral adipose tissue differences in black and white women. Am J Clin Nutr 61, 765771.
30Tittelbach TJ, Berman DM, Nicklas BJ, Ryan AS & Goldberg AP (2004) Racial differences in adipocyte size and relationship to the metabolic syndrome in obese women. Obes Res 12, 990998.
31Cossrow N & Falkner B (2004) Race/ethnic issues in obesity and obesity-related comorbidities. J Clin Endocrinol Metab 89, 25902594.
32Nielsen S, Guo ZK, Albu JB, Klein S, O'Brien PC & Jensen MD (2003) Energy expenditure, sex, and endogenous fuel availability in humans. J Clin Invest 111, 981988.
33Votruba SB & Jensen MD (2006) Sex-specific differences in leg fat uptake are revealed with a high-fat meal. Am J Physiol Endocrinol Metab 291, E1115E1123.
34Lamont LS, McCullough AJ & Kalhan SC (2001) Gender differences in leucine, but not lysine, kinetics. J Appl Physiol 91, 357362.
35Lamont LS (2005) Gender differences in amino acid use during endurance exercise. Nutr Rev 63, 419422.
36Hamadeh MJ, Devries MC & Tarnopolsky MA (2005) Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J Clin Endocrinol Metab 90, 35923599.
37Woodhouse LJ, Gupta N, Bhasin M, Singh AB, Ross R, Phillips J & Bhasin S (2004) Dose-dependent effects of testosterone on regional adipose tissue distribution in healthy young men. J Clin Endocrinol Metab 89, 718726.
38Singh R, Artaza JN, Taylor WE, Braga M, Yuan X, Gonzalez-Cadavid NF & Bhasin S (2006) Testosterone inhibits adipogenic differentiation in 3T3-L1 cells: nuclear translocation of androgen receptor complex with β-catenin and T-cell factor 4 may bypass canonical Wnt signaling to down-regulate adipogenic transcription factors. Endocrinology 147, 141154.
39Anderson LA, McTernan PG, Barnett AH & Kumar S (2001) The effects of androgens and estrogens on preadipocyte proliferation in human adipose tissue: influence of gender and site. J Clin Endocrinol Metab 86, 50455051.
40Tchernof A, Desmeules A, Richard C, Laberge P, Daris M, Mailloux J, Rheaume C & Dupont P (2004) Ovarian hormone status and abdominal visceral adipose tissue metabolism. J Clin Endocrinol Metab 89, 34253430.
41Pedersen SB, Kristensen K, Hermann PA, Katzenellenbogen JA & Richelsen B (2004) Estrogen controls lipolysis by up-regulating α2A-adrenergic receptors directly in human adipose tissue through the estrogen receptor α. Implications for the female fat distribution. J Clin Endocrinol Metab 89, 18691878.
42Rodriguez-Cuenca S, Monjo M, Proenza AM & Roca P (2005) Depot differences in steroid receptor expression in adipose tissue: possible role of the local steroid milieu. Am J Physiol Endocrinol Metab 288, E200E207.
43Richelsen B (1986) Increased α 2- but similar β-adrenergic receptor activities in subcutaneous gluteal adipocytes from females compared with males. Eur J Clin Invest 16, 302309.
44Kershaw EE & Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89, 25482556.
45Andrew R, Phillips DIW & Walker BR (1998) Obesity and gender influence cortisol secretion and metabolism in man. J Clin Endocrinol Metab 83, 18061809.
46Rask E, Walker BR, Söderber S, Livingstone DEW, Eliasson M, Johnson O, Andrew R & Olsson T (2002) Tissue-specific changes in peripheral cortisol metabolism in obese women: increased adipose 11β-hydroxysteroid dehydrogenase type 1 activity. J Clin Endocrinol Metab 87, 33303336.
47Stewart PM, Boulton A, Kumar S, Clark PMS & Shakleton CHL (1999) Cortisol metabolism in human obesity: impaired cortisone to cortisol conversion in subjects with central obesity. J Clin Endocrinol Metab 84, 10221027.
48Rask E, Olsson T, Söderber S, Andrew R, Livingstone DEW, Johnson O & Walker BR (2001) Tissue-specific dysregulation of cortisol metabolism in human obesity. J Clin Endocrinol Metab 86, 14181421.
49Hallschmid M, Benedict C, Schultes B, Fem H-L, Born J & Kern W (2004) Intranasal insulin reduces body fat in men but not in women. Diabetes 53, 30243029.
50Clegg DJ, Riedy CA, Smith KA, Benoit SC & Woods SC (2003) Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 52, 682687.
51Clegg DJ, Brown LM, Woods SC & Benoit SC (2006) Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55, 978987.
52Sierra-Johnson J, Johnson BD, Bailey KR & Turner ST (2004) Relationships between insulin sensitivity and measures of body fat in asymptomatic men and women. Obes Res 12, 20702077.
53Einstein FH, Atzmon G, Yang X-M, Ma X-H, Rincon M, Rudin E, Muzumdar R & Barzilai N (2005) Differential responses of visceral and subcutaneous fat depots to nutrients. Diabetes 54, 672678.
54Alexe D-M, Syridou G & Petridou ET (2006) Determinants of early life leptin levels and later life degenerative outcomes. Clin Med Res 4, 326335.
55Ostlund RE, Yang JW, Klein S & Gingerich R (1996) Relation between plasma leptin concentration and body fat, gender, diet, age, and metabolic covariates. J Clin Endocrinol Metab 81, 39093913.
56Rosenbaum M, Nicolson M, Hirsch J, Heymsfield SB, Gallagher D, Chu F & Leibel RL (1996) Effects of gender, body composition, and menopause on plasma concentrations of leptin. J Clin Endocrinol Metab 81, 34243427.
57Kennedy A, Gettys TW, Watson P, Wallace P, Ganaway E, Pan Q & Garvey WT (1997) The metabolic significance of leptin in humans: gender-based differences in relationship to adiposity, insulin sensitivity, and energy expenditure. J Clin Endocrinol Metab 82, 12931300.
58Saad MF, Damani S, Gingerich RL, Riad-Gabriel MG, Khan A, Boyadjian R, Jinagouda SD, El-Tawil K, Rude RK & Kamdar V (1997) Sexual dimorphism in plasma leptin concentration. J Clin Endocrinol Metab 82, 579584.
59Casabiell X, Piñeiro V, Peino R, Lage M, Camiña J, Gallego R, Vallejo LG, Dieguez C & Casanueva FF (1998) Gender differences in both spontaneous and stimulated leptin secretion by human omental adipose tissue in vitro: dexamethasone and estradiol stimulate leptin release in women, but not in men. J Clin Endocrinol Metab 83, 21492155.
60Chehab FF, Lim ME & Lu R (1996) Correction of the sterility defect in homozygous obese female mice by treatment with human recombinant leptin. Nat Genet 12, 318320.
61Ashworth CJ, Hoggard N, Thomas L, Mercer JG, Wallace JM & Lea RG (2000) Placental leptin. Rev Reprod 5, 1824.
62Leperq J, Challier JC, Guerre-Millo M, Cauzac M, Vidal H & Haugel-de Mouzon S (2001) Prenatal leptin production: evidence that fetal adipose tissue produces leptin. J Clin Endocrinol Metab 86, 24092413.
63Henson MC & Castracane VD (2006) Leptin in pregnancy: an update. Biol Reprod 74, 218229.
64Aquila S, Gentile M, Middea E, Catalano S, Morelli C, Pezzi V & Andò S (2005) Leptin secretion by human ejaculated spermatozoa. J Clin Endocrinol Metab 90, 47534761.
65McDowell MA, Brody DJ & Hughs JP (2007) Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999–2004. J Adolescent Health 40, 227231.
66Lee JM, Appugliese D, Kaciroti N, Corwyn RF, Bradley RH & Lumeng JC (2007) Weight status in young girls and the onset of puberty. Pediatrics 119, e624e630.
67Hauguel-de Mouzon S, Lepercq J & Catalano P (2006) The known and unknown of leptin in pregnancy. Am J Obstet Gynecol 194, 15371545.
68Jakimiuk AJ, Skalba P, Huterski R, Haczynski J & Magoffin DA (2003) Leptin messenger ribonucleic acid (mRNA) content in the human placenta at term: relationship to levels of leptin in cord blood and placental weight. Gynecol Endocrinol 17, 311316.
69Henson MC & Castracane VD (2000) Leptin in pregnancy. Biol Reprod 63, 12191228.
70Sooranna SR, Ward S & Bajoria R (2001) Fetal leptin influences birth weight in twins with discordant growth. Pediatr Res 49, 667672.
71Henson MC, Swan KF, Edwards DE, Hoyle GW, Purcell J & Castracane VD (2004) Leptin receptor in fetal lung increases in late gestation in the baboon: a model for human pregnancy. Reproduction 127, 8994.
72Speakman JR (2007) A nonadaptive scenario explaining the genetic predisposition to obesity: the “predation release” hypothesis. Cell Metab 6, 511.
73Speakman JR (2006) The genetics of obesity: five fundamental problems with the famine hypothesis. In Adipose Tissue and Adipokines in Health and Disease, pp. 221236 [Fantuzzi G and Mazzone T, editors]. New York: Humana Press.
74Sallmén M, Sandler DP, Hoppin JA, Blair A & Baird DD (2006) Reduced fertility among overweight and obese men. Epidemiology 17, 520523.
75Jasienska G, Ziomkiewicz A, Lipson SF, Thune I & Ellison PT (2005) High ponderal index at birth predicts high estradiol levels in adult women. Am J Hum Biol 18, 133140.
76Jasienska G, Thune I & Ellison PT (2006) Fatness at birth predicts adult susceptibility to ovarian suppression: an empirical test of the Predictive Adaptive Response hypothesis. PNAS 103, 1275912762.
77Berk ES, Kovera AJ, Boozer CN, Pi-Sunyer FX & Albu JB (2006) Metabolic inflexibility in substrate use is present in African-American but not Caucasian healthy, premenopausal, nondiabetic women. J Clin Endocrinol Metab 91, 40994106.
78Cogswell ME, Perry GS, Schieve LA & Dietz WH (2001) Obesity in women of childbearing age: risks, prevention, and treatment. Prim Care Update Ob Gyns 8, 89105.
79Yu CK, Teoh TG & Robinson S (2006) Obesity in pregnancy. BJOG 113, 11171125.
80Catalano PM & Ehrenberg HM (2006) The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG 113, 11261133.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 203
Total number of PDF views: 795 *
Loading metrics...

Abstract views

Total abstract views: 1982 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 26th February 2018. This data will be updated every 24 hours.