Waist-hip ratio and cognitive ability: is gluteofemoral fat a privileged store of neurodevelopmental resources?

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Abstract

Upper-body fat has negative effects and lower-body fat has positive effects on the supply of long-chain polyunsaturated fatty acids that are essential for neurodevelopment. Thus, waist-hip ratio (WHR), a useful proxy for the ratio of upper-body fat to lower-body fat, should predict cognitive ability in women and their offspring. Moreover, because teenage mothers and their children compete for these resources, their cognitive development should be compromised, but less so for mothers with lower WHRs. These predictions are supported by data from the Third National Health and Nutrition Examination Survey. Controlling for other correlates of cognitive ability, women with lower WHRs and their children have significantly higher cognitive test scores, and teenage mothers with lower WHRs and their children are protected from cognitive decrements associated with teen births. These findings support the idea that WHR reflects the availability of neurodevelopmental resources and thus offer a new explanation for men's preference for low WHR.

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)

  • B. Imani et al.

    A nomogram to predict the probability of live birth after clomiphene citrate induction of ovulation in normogonadotropic oligoamenorrheic infertility

    Fertility and Sterility

    (2002)
  • C. Klein-Platat et al.

    Plasma fatty acid composition is associated with the metabolic syndrome and low-grade inflammation in overweight adolescents

    American Journal of Clinical Nutrition

    (2005)
  • F. Marlowe et al.

    Preferred waist-to-hip ratio and ecology

    Personality and Individual Differences

    (2001)
  • M. Pall et al.

    Family size in women with polycystic ovary syndrome

    Fertility and Sterility

    (2006)
  • S.D. Phinney et al.

    Human subcutaneous adipose tissue shows site-specific differences in fatty acid composition

    American Journal of Clinical Nutrition

    (1994)
  • D. Singh et al.

    Beauty is in the eye of the plastic surgeon: Waist–hip ratio (WHR) and women's attractiveness

    Personality and Individual Differences

    (2007)
  • L.S. Sugiyama

    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

    (2004)
  • M.J. Tovee et al.

    Supermodels: stick insects or hourglasses?

    Lancet

    (1997)
  • M.H.A. van Hooff et al.

    Polycystic ovaries in adolescents and the relationship with menstrual cycle patterns, luteinizing hormone, androgens, and insulin

    Fertility and Sterility

    (2000)
  • A. Wetsman et al.

    How universal are preferences for female waist-to-hip ratios? Evidence from the Hadza of Tanzania

    Evolution and Human Behavior

    (1999)
  • F. Yang et al.

    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

    (2006)
  • M.D. Al et al.

    Relation between birth order and the maternal and neonatal docosahexaenoic acid status

    European Journal of Clinical Nutrition

    (1997)
  • M.B. Andersson

    Sexual selection

    (1994)
  • P. Bjorntorp

    The association between obesity, adipose tissue distribution and disease

    Acta Medica Scandinavia

    (1988)
  • P.J. Brown et al.

    An anthropological perspective on obesity

    Annals of the New York Academy of Sciences

    (1987)
  • J.G.H. Cant

    Hypothesis for the evolution of human breasts and buttocks

    American Naturalist

    (1981)
  • W.C. Chumlea et al.

    Body composition estimates from NHANES III bioelectrical impedance data

    International Journal of Obesity

    (2002)
  • J.T. Cohen et al.

    A quantitative analysis of prenatal intake of n−3 polyunsaturated fatty acids and cognitive development

    American Journal of Preventive Medicine

    (2005)
  • T. Decsi et al.

    Polyunsaturated fatty acids in plasma lipids of obese children with and without metabolic cardiovascular syndrome

    Lipids

    (2000)
  • T. Decsi et al.

    Long-chain polyunsaturated fatty acids in plasma lipids of obese children

    Lipids

    (1996)
  • M. Del Prado et al.

    Contribution of dietary and newly formed arachidonic acid to milk secretion in women in low fat diets

    Advances in Experimental Medicine and Biology

    (2000)
  • B.J. Dixson et al.

    Studies of human physique and sexual attractiveness: Sexual preferences of men and women in China

    American Journal of Human Biology

    (2007)
  • D.B. Downey

    Number of siblings and intellectual development: The resource dilution explanation

    American Psychologist

    (2001)
  • D.L. Dufour et al.

    Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation

    American Journal of Human Biology

    (2002)
  • S.B. Eaton et al.

    Paleolithic nutrition revisited: A twelve-year retrospective on its nature and implications

    European Journal of Clinical Nutrition

    (1997)
  • M.J.C. Eijkemans et al.

    High singleton live birth rate following classical ovulation induction in normogonadotrophic anovulatory infertility

    Human Reproduction

    (2003)
  • A.M. Fredriks et al.

    Are age references for waist circumference, hip circumference and waist–hip ratio in Dutch children useful in clinical practice?

    European Journal of Pediatrics

    (2005)
  • R.E. Frisch

    Pubertal adipose tissue: Is it necessary for normal sexual maturation? Evidence from the rat and human female

    Federation Proceedings

    (1980)
  • A. Furnham et al.

    Cross cultural differences in the perception of female body shapes

    International Journal of Eating Disorders

    (1994)
  • A. Furnham et al.

    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

    (2003)
  • B.J. Fuhrman et al.

    Erythrocyte membrane phospholipid composition as a biomarker of dietary fat

    Annals of Nutrition and Metabolism

    (2006)
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