Waist-hip ratio and cognitive ability: is gluteofemoral fat a privileged store of neurodevelopmental resources?
Introduction
Compared with men and other female primates in the wild (Dufour & Slather, 2002), women have substantially more total body fat; the effect size (d) for the human sex difference is 2.6 at the end of puberty (Boot, Bouquet, de Ridder, Krenning, & de Muinck Keizer-Shrama, 1997). Body fat distribution is also highly dimorphic, with women having more gluteofemoral fat and less abdominal and visceral fat than men, resulting in lower waist-hip ratios (WHRs), with an effect size of 1.7 (Tichet, Vol, Balkau, Le Clesiau, & D'Hour, 1993).
Dimorphic body fat distribution, as reflected in WHR, seems to be an important dimension of female attractiveness. Many studies have shown that men in Western countries prefer women with both a low WHR (0.6–0.7) and a low body mass index (BMI; 17–20) (Singh, 1993, Sugiyama, 2005; Tovee, Maisey, Emery & Cornelisson, 1999; Wilson, 2005). For women who are considered to be highly attractive, the mean WHR and BMI were 0.68±0.04 and 18.09±1.21, respectively, in 300 Playboy models (Tovee et al., 1997), and 0.68±0.04 and 18.4±1.3, respectively, in 129 female adult film stars (Voracek & Fisher, 2006).
Several studies in non-Western populations also show a preference for low WHRs, even in some cases where heavier figures are preferred. A sample of Japanese men showed a stronger preference for low WHR then men in Britain (Swami, Caprario, Tovee, & Furnham, 2006), and men in a Chinese study showed a preference for a WHR of 0.6 (Dixson, Dixson, Li, & Anderson, 2007). Furnham, Moutafi, and Baguma (2002) found that male Ugandan students preferred a WHR of 0.5 while preferring heavier body weight. Furnham, McClelland, and Omer (2003) found that young men in Kenya also preferred figures with a narrow waist, as did Sugiyama (2004) for the Shiwiar of Ecuador. More systematically, using data for 58 cultures in the Human Area Relations Files, Brown and Konner (1987) found that fatter legs and hips in females were valued in 90%.
Males in two isolated populations have shown a preference for larger WHRs. Using frontal views, Marlowe and Wetsman (2001) and Wetsman and Marlowe (1999) found that Hadza men preferred women with wider WHRs. Also using frontal views, Yu and Shepard (1998) found that men in an isolated Matsigenka village in Peru ranked an overweight figure with a WHR of 0.9 as most attractive, but noted that this WHR was characteristic of young women in the village before their first pregnancy. In contrast, they found that Matsigenka men in less isolated villages were indistinguishable from American men in their WHR preference. Neither of these studies tested for preference for larger buttocks in lateral views, which Goodwin (2001) found were preferred by African Americans. But in a later Hadza study (Marlowe, Apicella, & Reed, 2005), compared to American men, Hazda men showed a stronger preference for low WHR in lateral views, suggesting that the earlier studies may have overestimated the difference between American and Hadza men's WHR preferences.
In contrast to a fairly widespread preference for lower WHRs, cross-cultural studies have not supported a universal male preference for women with low BMIs. Furnham and Baguma (1994) found that Ugandan men rated obese figures as more attractive than British men. Furnham et al. (2002) found that male Ugandan students also preferred a heavier to a lighter figure (but rated women with a WHR of 0.5 as most attractive). Jackson and McGill (1997) found that most African-American men preferred women of “average” weight (136 lb), while a majority of white males preferred women who were thinner than average. Wetsman and Marlowe (1999) found that Hadza men preferred women with heavier figures, and Shiwar men in Ecuador also preferred heavier women within their population (Sugiyama, 2004, Sugiyama, 2005). Men in Gambia also preferred heavier women compared to African Americans and white Americans (Siervo, Grey, Nyan, & Prentice, 2006). Perhaps most tellingly, Brown and Konner (1987) found that people in 81% of 58 cultures valued plump or moderately fat women versus 19% preferring thin women. Hungry men also prefer heavier women (Swami & Tovee, 2006).
Precisely what proportion of the variance in female bodily attractiveness is explained by low BMI or low WHR is the subject of ongoing debate (Singh & Randall, 2007; Tovee, Hancock, Mahmoodi, Singleton, & Cornelissen, 2002; Tovee et al., 1999, Yu & Shepard, 1998). This issue is complicated both by the fact that the two parameters naturally covary and by the possibility that one or both of the preferences may differ among populations either adaptively (e.g., related to the risk of food shortage; Sugiyama, 2004, Swami & Tovee, 2006) or nonadaptively (e.g., “fashion”; Kowner, 2002). Regardless, a preference for low WHR seems widespread and strong enough to warrant questions about its possible adaptive bases.
Preferences often evolve when a perceptual signal is correlated with an underlying fitness-enhancing trait (Andersson, 1994). What might a low WHR signal? Arguments to date have focused mainly on the possibility that WHR may be correlated with fertility and/or health (Marlowe et al., 2005, Pawlowski & Dunbar, 2005, Singh, 1993, Sugiyama, 2005), but both of these assertions rest on evidence that is either limited or of questionable relevance.
Some studies of in vitro fertilization show that women with a WHR of <0.80 have a higher probability of “conceiving” (Imani et al., 2002, Van Noord-Zaadstra et al., 1991, Wass et al., 1997, Zaadstra et al., 1993), but a similar study failed to find any relationship between a woman's WHR and her likelihood of conceiving with vaginal insemination (Eijkemans, Imani, Mulders, Habbema, & Fauser, 2003). Indirect support for the fertility hypothesis is provided by evidence that women with very high WHRs (>0.85) have more anovulatory cycles (Moran et al., 1999). Similarly, another study showed higher levels of estradiol and progesterone with low WHR, but only in those with larger breast size (Jasienska, Ziomkiewicz, Ellison, Lipson, & Thune, 2004). Many of these studies fail to control for BMI, which covaries with WHR (Tovee et al., 1999), so they likely include obese women with polycystic ovarian syndrome (PCOS), many of whom have lower hormone levels and impaired fertility (Pasquali, Gambineri, & Pagotto, 2006). However, normal-weight PCOS patients may have enhanced fertility (Gleicher & Barad, 2006), and there is no difference in primary family size between PCOS patients and controls (Pall, Stephens, & Azziz, 2006).
Regardless of the relation with PCOS, several studies suggest that WHR does not identify young women with menstrual disorders linked to infertility. In a study of 22,480 adolescents aged 15–16 years, there was no difference in WHR between those with regular cycles and those with oligomenorrhea or irregular menses (van Hooff, Voorhorst, Kaptein, & Hirasing, 1999), and the same was true in two other independent studies of young women aged 16–17 and 15–18 years (van Hooff et al., 2000a, Van Hooff et al., 2000b).
There has also been little discussion of any pathway through which a low WHR might enhance fertility. Some suggest that fat stores help supply the energy needs of pregnancy and lactation (Cant, 1981, Frisch, 1980, Sugiyama, 2005), but women with lower WHRs usually have lower total fat stores (Yang et al., 2006; see below). Moreover, this view does not explain why fat would be preferentially stored on the hips and thighs, nor why similar sex differences in body fat are not generally found in mammals (Lassek & Gaulin, 2007).
It has also been suggested that a low WHR signals better health (Marlowe et al., 2005, Pawlowski & Dunbar, 2005, Singh, 1993, Sugiyama, 2005). This claim is supported by abundant evidence indicating that higher WHRs are associated with increased morbidity and mortality (Bjorntorp, 1988). However, this finding is based on relatively affluent postmenopausal women who are most commonly afflicted with chronic diseases that were probably rare during the Paleolithic (Eaton, Eaton, & Konner, 1997). “Thrifty genes” promoting abdominal obesity may also have had survival value in populations subject to nutritional stress (Groop, 2000), but which only recently have become responsible for many of the adverse effects associated with high WHRs. Thus, it is not clear whether, over most of human evolution, low- and high-WHR females would have differed in survival during their reproductive years.
If WHR is not a reliable predictor of fertility or survival during the reproductive years, are there other reasons why it evolved as a criterion of male mate choice and why females preferentially store fat in the gluteofemoral depot? We have been pursuing the hypothesis that gluteofemoral fat and abdominal fat have opposite effects on the availability of essential fatty acids needed for fetal and infant brain development, with lower-body fat increasing the supply of these neurodevelopment resources and with upper-body fat inhibiting their availability, as discussed below. If this is correct, male preference for lower WHRs would likely spread in a species undergoing rapid brain expansion and, hence, increased demand for brain-building resources.
Storing gluteofemoral fat is a high priority during human female development. Most of the 10–20 kg of fat stored during a female's childhood and puberty is gluteofemoral fat (Fredriks et al., 2005, Hammer et al., 1991). Importantly, menarche is accelerated by a greater proportion of gluteofemoral fat and is slowed by higher levels of abdominal fat (Lassek & Gaulin, 2007). Moreover, even with restricted food intake, gluteofemoral fat is metabolically protected from use until late pregnancy and lactation (the period of maximal infant brain growth) when it is selectively mobilized (Rebuffe-Scrive, 1987, Rebuffe-Scrive et al., 1985).
Gluteofemoral fat is the main source of long-chain polyunsaturated fatty acids (LCPUFAs), especially the omega-3 docosahexaenoic acid (DHA), that are critical for fetal and infant brain development, and these LCPUFAs make up approximately 20% of the dry weight of the human brain (Del Prado et al., 2000, Demmelmair et al., 1998, Fidler et al., 2000, Hachey et al., 1987). A recent meta-analysis estimates that a child's IQ increases by 0.13 point for every 100-mg increase in daily maternal prenatal intake of DHA (Cohen, Bellinger, Connor, & Shaywitz, 2005), and a recent study in England shows a similar positive relationship between a mother's prenatal consumption of seafood (high in DHA) and her child's verbal IQ (Hibbeln et al., 2007).
Gluteofemoral fat is richer than abdominal and visceral fat in essential LCPUFAs (Phinney et al., 1994, Pittet et al., 1979, Shafer & Overvad, 1990), and a lower WHR is associated with higher DHA levels in the blood (Decsi et al., 1996, Garaulet et al., 2001, Karlsson et al., 2006, Klein-Platat et al., 2005, Seidell et al., 1991). In contrast, abdominal fat decreases the amount of the enzyme Δ-5 desaturase, which is rate limiting for the synthesis of neurologically important LCPUFAs from dietary precursors (Fuhrman et al., 2006, Phinney, 1996), and higher WHRs decrease DHA production (Decsi et al., 2000, Hollmann et al., 1997). Studies using isotope-labeled fatty acids show that 60–80% of LCPUFAs in human breast milk come from maternal fat stores, rather than from the mother's current dietary intake (Del Prado et al., 2000, Demmelmair et al., 1998, Fidler et al., 2000, Hachey et al., 1987), presumably because of the rapid rate of infant brain development relative to limited dietary supplies of LCPUFAs.
Each cycle of pregnancy and lactation draws down the gluteofemoral fat store deposited in early life; in many poorly nourished populations, this fat is not replaced, and women become progressively thinner with each pregnancy, which is termed “maternal depletion” (Lassek & Gaulin, 2006). We have recently shown that even well-nourished American women experience a relative loss of gluteofemoral fat with parity (Lassek & Gaulin, 2006). In parallel, parity is inversely related to the amount of DHA in the blood of mothers and neonates (Al, van Houwelingen, & Hornstra, 1997).
That critical fatty acids are depleted with parity is also consistent with studies showing that cognitive functioning is impaired with parity. IQ is negatively correlated with birth order (Downey, 2001), and twins have decreased DHA (McFadyen, Farquharson, & Cockburn, 2001) and compromised neurodevelopment compared to singletons (Ronalds, De Stavola, & Leon, 2005). The mother's brain also typically decreases in size during pregnancy (Oatridge et al., 2002).
Women who become pregnant while they are still growing have a three-way conflict over nutritional resources that are needed to develop their own brains, nutritional resources that are to be stored for future pregnancies, and the needs of the current fetus; as a result, cognitive development in their offspring is often impaired (Furstenberg et al., 1987).
Only two previous studies have explored the relationship between WHR and cognitive ability, and they have shown that, in older men and women, higher WHRs are associated with poorer cognitive performance and detrimental changes in the brain (Jagust et al., 2005, Waldstein & Katzel, 2006).
Taken altogether, these facts suggest that the unusual fattiness and fat deposition patterns of reproductive-aged women may be the result of natural selection for the ability to support fetal and infant neurodevelopment—a selection pressure that was much weaker in our close primate relatives. This hypothesis thus unites two derived (evolutionarily novel) features of Homo sapiens: sexually dimorphic fat distributions and large brains. On this view, a low WHR signals the availability of critical brain-building resources and should therefore have consequences for cognitive performance.
Three predictions follow:
- (a)
A woman's WHR should be negatively correlated with her offspring's cognitive abilities.
- (b)
Because mothers pass both DHA and genes affecting LCPUFA metabolism (and hence WHR) to their (female) offspring and because WHR reflects the availability of LCPUFA, a woman's WHR should also be negatively correlated with her own cognitive abilities.
- (c)
Since mothers and offspring will be in competition for LCPUFAs and since this competition will be more intense while she is still growing her own brain and when her own LCPUFA reserves are low, cognitive development should be impaired in women whose first birth occurred early and in the resulting offspring, but lower WHRs, indicating larger LCPUFA stores, should be significantly protective for both.
We tested these predictions using anthropometric, demographic, and cognitive data from the Third National Health and Nutrition Examination Survey (NHANES III), which was conducted by the US National Center for Health Statistics from 1988 to 1994.
Section snippets
Methods
The NHANES III sample included 16,325 females aged 0–90 years (mean age, 29.9±25.8 years), with 38% non-Hispanic whites, 29% non-Hispanic blacks, 28% Hispanics, and 5% other. Anthropometric data included waist and hip circumferences, WHR, BMI, and total body fat estimated from bioelectrical impedance (Chumlea, Guo, Kuczmarski, Flegal, & Johnson, 2002). Sociodemographic data included years of education, race/ethnicity, and family income.
We analyzed data from seven subsamples:
- 1.
1933 mothers
Relationship between WHR, BMI, and total body fat
For 752 nulligravidas aged 18–29 years (average age, 21.9±3.2 years), WHR explains 23% of the variance in total body fat estimated from bioelectrical impedance. Controlling for age and race/ethnicity, an increase of 0.01 in WHR increases total body fat by 0.83 kg. Similarly, WHR explains 28% of the variance in BMI, with an increase of 0.47 kg/m2 for an increase of 0.01 in WHR. BMI explains 89% of the variance in estimated body fat; an increase of 1 kg/m2 increases fat by 1.8 kg; when added to
WHR, BMI, and body fat
WHR is strongly positively related to body fat and BMI in young nulligravidas. BMI is very strongly related to body fat, and the relationship of WHR to BMI mediates the relationship of WHR with fat. Since women with low WHRs and BMIs generally have less body fat, they have less energy reserves to support the energy demands of pregnancy and to increase survival in times of famine, suggesting that female energy stores are not a major factor in male preferences for low WHRs. However the debate is
Acknowledgments
We appreciate the review, comments, and suggestions of John Tooby, Leda Cosmides, Martie Haselton, Mike Gurven, Jim Roney, Carolyn Hodges, Kate Hanson, Danielle Truxaw, Natalie Brechtel, Lisa Weber, Dan Fessler, and two anonymous reviewers.
References (83)
- et al.
Temporal changes in dietary fats: Role of n−6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity
Progress in Lipid Research
(2006) - et al.
Determinants of body composition measured by dual-energy X-ray absorptiometry in Dutch children and adolescents
American Journal of Clinical Nutrition
(1997) - et al.
Metabolism of U13C-labeled linoleic acid in lactating women
Journal of Lipid Research
(1998) - et al.
Docosahexaenoic acid transfer into human milk after dietary supplementation: A randomized clinical trial
Journal of Lipid Research
(2000) - et al.
A cross-cultural study on the role of weight and waist-to-hip ratio on female attractiveness
Personality and Individual Differences
(2002) - et al.
Site-specific differences in the fatty acid composition of abdominal adipose tissue in an obese population from a Mediterranean area
American Journal of Clinical Nutrition
(2001) - et al.
An evolutionary concept of polycystic ovarian disease: Does evolution favour reproductive success over survival?
Reproductive Biomedicine Online
(2006) - et al.
Human lactation: maternal transfer of dietary triglycerides labeled with stable isotopes
Journal of Lipid Research
(1987) - et al.
Impact of pubertal development on body fat distribution among white, Hispanic, and Asian female adolescents
Journal of Pediatrics
(1991) - et al.
Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study
Lancet
(2007)
A nomogram to predict the probability of live birth after clomiphene citrate induction of ovulation in normogonadotropic oligoamenorrheic infertility
Fertility and Sterility
Plasma fatty acid composition is associated with the metabolic syndrome and low-grade inflammation in overweight adolescents
American Journal of Clinical Nutrition
Preferred waist-to-hip ratio and ecology
Personality and Individual Differences
Family size in women with polycystic ovary syndrome
Fertility and Sterility
Human subcutaneous adipose tissue shows site-specific differences in fatty acid composition
American Journal of Clinical Nutrition
Beauty is in the eye of the plastic surgeon: Waist–hip ratio (WHR) and women's attractiveness
Personality and Individual Differences
Is beauty in the context-sensitive adaptations of the beholder? Shiwiar use of waist-to-hip ratio in assessments of female mate value
Evolution and Human Behavior
Supermodels: stick insects or hourglasses?
Lancet
Polycystic ovaries in adolescents and the relationship with menstrual cycle patterns, luteinizing hormone, androgens, and insulin
Fertility and Sterility
How universal are preferences for female waist-to-hip ratios? Evidence from the Hadza of Tanzania
Evolution and Human Behavior
Receiver-operating characteristic analyses of body mass index, waist circumference and waist-to-hip ratio for obesity: Screening in young adults in central south of China
Clinical Nutrition
Relation between birth order and the maternal and neonatal docosahexaenoic acid status
European Journal of Clinical Nutrition
Sexual selection
The association between obesity, adipose tissue distribution and disease
Acta Medica Scandinavia
An anthropological perspective on obesity
Annals of the New York Academy of Sciences
Hypothesis for the evolution of human breasts and buttocks
American Naturalist
Body composition estimates from NHANES III bioelectrical impedance data
International Journal of Obesity
A quantitative analysis of prenatal intake of n−3 polyunsaturated fatty acids and cognitive development
American Journal of Preventive Medicine
Polyunsaturated fatty acids in plasma lipids of obese children with and without metabolic cardiovascular syndrome
Lipids
Long-chain polyunsaturated fatty acids in plasma lipids of obese children
Lipids
Contribution of dietary and newly formed arachidonic acid to milk secretion in women in low fat diets
Advances in Experimental Medicine and Biology
Studies of human physique and sexual attractiveness: Sexual preferences of men and women in China
American Journal of Human Biology
Number of siblings and intellectual development: The resource dilution explanation
American Psychologist
Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation
American Journal of Human Biology
Paleolithic nutrition revisited: A twelve-year retrospective on its nature and implications
European Journal of Clinical Nutrition
High singleton live birth rate following classical ovulation induction in normogonadotrophic anovulatory infertility
Human Reproduction
Are age references for waist circumference, hip circumference and waist–hip ratio in Dutch children useful in clinical practice?
European Journal of Pediatrics
Pubertal adipose tissue: Is it necessary for normal sexual maturation? Evidence from the rat and human female
Federation Proceedings
Cross cultural differences in the perception of female body shapes
International Journal of Eating Disorders
A cross cultural comparison of ratings of perceived fecundity and sexual attractiveness as a function of body weight and waist to hip ratio
Psychology, Health and Medicine
Erythrocyte membrane phospholipid composition as a biomarker of dietary fat
Annals of Nutrition and Metabolism
Cited by (101)
Toward capturing the functional and nuanced nature of social stereotypes: An affordance management approach
2020, Advances in Experimental Social PsychologyCitation Excerpt :That said, male bodies tend to prioritize the accumulation of abdominal fat whereas female bodies—especially the bodies of young, reproductive-aged women—tend to prioritize the accumulation of gluteofemoral fat (although women with overweight and obesity can present with either type of fat) (Krems, Barlev, & Becker, 2020). Although both types of fat provide stores of calories, women's gluteofemoral fat appears to have characteristics especially beneficial for conception, gestation, lactation, and offspring neurodevelopment (Ellison, 2003; Frisch, 2004; Jasieńska, 2001; Jasieńska, Ziomkiewicz, Ellison, Lipson, & Thune, 2004; Lassek & Gaulin, 2006, 2008). Evidence even suggests that such a pattern of fat distribution—specifically having an hourglass figure (fat in the breasts, hips, and thighs, and not in the abdomen)—might be an honest signal of female fecundity and reproductive potential (e.g., Lassek & Gaulin, 2019; Zaadstra et al., 1993).
Evidence supporting nubility and reproductive value as the key to human female physical attractiveness
2019, Evolution and Human BehaviorCitation Excerpt :This is concordant with our finding that parity was associated with lower plasma levels of DHA, consistent with earlier studies (Hornstra, 2000; Min et al., 2000). Jointly these observations support the idea that the highly derived human female gluteofemoral depot evolved to store DHA critical to fetal and infant neurodevelopment in our unusually large-brained species (Lassek & Gaulin, 2006, 2008). Consistent with this proposal, in our current sample, both lower waist/stature and lower waist/thigh ratios were associated with a higher percentage of DHA in plasma fatty acids.
Tendencies Toward Supernormality/Subnormality in Generating Attractive and Unattractive Female and Male Avatars: Gender Differences
2023, Archives of Sexual BehaviorExtensions of Sexual Strategies Theory across Peoples, Cultures, and Ecologies
2023, The Oxford Handbook of Human MatingWeight Location Moderates Weight-Based Self-Devaluation and Perceived Social Devaluation in Women
2022, Social Psychological and Personality Science