Sex differences in energy metabolism: natural selection, mechanisms and consequences

Darwin, C. On the Origin of Species (John Murray, 1859).

Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).

Frisch, R. E. & McArthur, J. W. Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185, 949–951 (1974).

Article  CAS  PubMed  Google Scholar 

Frisch, R. E. Body fat, menarche, fitness and fertility. Hum. Reprod. 2, 521–533 (1987).

Article  CAS  PubMed  Google Scholar 

Gerisch, B., Weitzel, C., Kober-Eisermann, C., Rottiers, V. & Antebi, A. A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev. Cell 1, 841–851 (2001).

Article  CAS  PubMed  Google Scholar 

Brüning, J. C. et al. Role of brain insulin receptor in control of body weight and reproduction. Science 289, 2122–2125 (2000).

Article  PubMed  Google Scholar 

Burks, D. J. et al. IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 407, 377–382 (2000).

Article  CAS  PubMed  Google Scholar 

Zhang, Y. et al. Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432 (1994).

Article  CAS  PubMed  Google Scholar 

Chehab, F. F., Lim, M. E. & Lu, R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat. Genet. 12, 318–320 (1996).

Article  CAS  PubMed  Google Scholar 

Ahima, R. S. et al. Role of leptin in the neuroendocrine response to fasting. Nature 382, 250–252 (1996).

Article  CAS  PubMed  Google Scholar 

Ahima, R. S., Dushay, J., Flier, S. N., Prabakaran, D. & Flier, J. S. Leptin accelerates the onset of puberty in normal female mice. J. Clin. Invest. 99, 391–395 (1997).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Paczoska-Eliasiewicz, H. E. et al. Exogenous leptin advances puberty in domestic hen. Domest. Anim. Endocrinol. 31, 211–226 (2006).

Article  CAS  PubMed  Google Scholar 

Paczoska-Eliasiewicz, H. E. et al. Attenuation by leptin of the effects of fasting on ovarian function in hens (Gallus domesticus). Reproduction 126, 739–751 (2003).

Article  CAS  PubMed  Google Scholar 

Ahmed, M. L., Ong, K. K. & Dunger, D. B. Childhood obesity and the timing of puberty. Trends Endocrinol. Metab. 20, 237–242 (2009).

Article  CAS  PubMed  Google Scholar 

Hoyenga, K. B. & Hoyenga, K. T. Gender and energy balance: sex differences in adaptations for feast and famine. Physiol. Behav. 28, 545–563 (1982).

Article  CAS  PubMed  Google Scholar 

Widdowson, E. M. The response of the sexes to nutritional stress. Proc. Nutr. Soc. 35, 175–180 (1976).

Article  CAS  PubMed  Google Scholar 

Della Torre, S. & Maggi, A. Sex differences: a resultant of an evolutionary pressure? Cell Metab. 25, 499–505 (2017).

Article  PubMed  Google Scholar 

Grayson, D. Differential mortality and the Donner Party disaster. Evol. Anthropol. 2, 151–159 (1993).

Article  Google Scholar 

Dols, M. J. & Van Arcken, D. J. Food supply and nutrition in the Netherlands during and immediately after World War II. Milbank Mem. Fund. Q. 24, 319–358 (1946).

Article  CAS  PubMed  Google Scholar 

Banning, C. Food shortage and public health, first half of 1945. Ann. Am. Acad. Pol. Soc. Sci. 245, 93–110 (1946).

Article  Google Scholar 

Zarulli, V. et al. Women live longer than men even during severe famines and epidemics. Proc. Natl Acad. Sci. USA 115, E832–E840 (2018).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Shi, H., Strader, A. D., Woods, S. C. & Seeley, R. J. Sexually dimorphic responses to fat loss after caloric restriction or surgical lipectomy. Am. J. Physiol. Endocrinol. Metab. 293, E316–E326 (2007).

Article  CAS  PubMed  Google Scholar 

Valle, A. et al. Sex-related differences in energy balance in response to caloric restriction. Am. J. Physiol. Endocrinol. Metab. 289, E15–E22 (2005).

Article  CAS  PubMed  Google Scholar 

Halsey, L. G. et al. Variability in energy expenditure is much greater in males than females. J. Hum. Evol. 171, 103229 (2022).

Article  PubMed  PubMed Central  Google Scholar 

Carter, S. L., Rennie, C. & Tarnopolsky, M. A. Substrate utilization during endurance exercise in men and women after endurance training. Am. J. Physiol. Endocrinol. Metab. 280, E898–E907 (2001).

Article  CAS  PubMed  Google Scholar 

Henderson, G. C. Sexual dimorphism in the effects of exercise on metabolism of lipids to support resting metabolism. Front. Endocrinol. 5, 162 (2014).

Google Scholar 

Horton, T. J., Pagliassotti, M. J., Hobbs, K. & Hill, J. O. Fuel metabolism in men and women during and after long-duration exercise. J. Appl. Physiol. 85, 1823–1832 (1998).

Article  CAS  PubMed  Google Scholar 

Tarnopolsky, M. A., Atkinson, S. A., Phillips, S. M. & MacDougall, J. D. Carbohydrate loading and metabolism during exercise in men and women. J. Appl. Physiol. 78, 1360–1368 (1995).

Article  CAS  PubMed  Google Scholar 

Braun, B. et al. Women at altitude: carbohydrate utilization during exercise at 4,300 m. J. Appl. Physiol. 88, 246–256 (2000).

Article  CAS  PubMed  Google Scholar 

Schmidt-Nielsen, K. Animal Physiology: Adaptation and Environment 5th edn (Cambridge Univ. Press, 1997).

Speechly, D. P., Taylor, S. R. & Rogers, G. G. Differences in ultra-endurance exercise in performance-matched male and female runners. Med. Sci. Sports Exerc. 28, 359–365 (1996).

CAS  PubMed  Google Scholar 

Bam, J., Noakes, T. D., Juritz, J. & Dennis, S. C. Could women outrun men in ultramarathon races? Med. Sci. Sports Exerc. 29, 244–247 (1997).

Article  CAS  PubMed  Google Scholar 

Hamadeh, M. J., Devries, M. C. & Tarnopolsky, M. A. Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J. Clin. Endocrinol. Metab. 90, 3592–3599 (2005).

Article  CAS  PubMed  Google Scholar 

Salehzadeh, F., Rune, A., Osler, M. & Al-Khalili, L. Testosterone or 17β-estradiol exposure reveals sex-specific effects on glucose and lipid metabolism in human myotubes. J. Endocrinol. 210, 219–229 (2011).

Article  CAS  PubMed  Google Scholar 

Maher, A. C., Akhtar, M. & Tarnopolsky, M. A. Men supplemented with 17β-estradiol have increased β-oxidation capacity in skeletal muscle. Physiol. Genomics 42, 342–347 (2010).

Article  CAS  PubMed  Google Scholar 

Ribas, V. et al. Skeletal muscle action of estrogen receptor α is critical for the maintenance of mitochondrial function and metabolic homeostasis in females. Sci. Transl. Med. 8, 334ra354 (2016).

Article  Google Scholar 

Donnelly, J. E. et al. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch. Intern. Med. 163, 1343–1350 (2003).

Article  PubMed  Google Scholar 

Pietrobelli, A. et al. Sexual dimorphism in the energy content of weight change. Int. J. Obes. Relat. Metab. Disord. 26, 1339–1348 (2002).

Article  CAS  PubMed  Google Scholar 

Nielsen, S. et al. Energy expenditure, sex, and endogenous fuel availability in humans. J. Clin. Invest. 111, 981–988 (2003).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Henderson, G. C. et al. Lipolysis and fatty acid metabolism in men and women during the postexercise recovery period. J. Physiol. 584, 963–981 (2007).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Uranga, A. P., Levine, J. & Jensen, M. Isotope tracer measures of meal fatty acid metabolism: reproducibility and effects of the menstrual cycle. Am. J. Physiol. Endocrinol. Metab. 288, E547–E555 (2005).

Article  CAS  PubMed  Google Scholar 

O’Sullivan, A. J., Crampton, L. J., Freund, J. & Ho, K. K. The route of estrogen replacement therapy confers divergent effects on substrate oxidation and body composition in postmenopausal women. J. Clin. Invest. 102, 1035–1040 (1998).

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