Evidence supporting nubility and reproductive value as the key to human female physical attractiveness

Abstract

Selection should favor mating preferences that increase the chooser's reproductive success. Many previous studies have shown that the women men find most attractive in well-nourished populations have low body mass indices (BMIs) and small waist sizes combined with relatively large hips, resulting in low waist-hip ratios (WHRs). A frequently proposed explanation for these preferences is that such women may have enhanced health and fertility; but extensive evidence contradicts this health-and-fertility explanation. An alternative view is that men are attracted to signs of nubility and high reproductive value, i.e., by indicators of physical and sexual maturity in young women who have not been pregnant. Here we provide evidence in support of the view that a small waist size together with a low WHR and BMI is a strong and reliable sign of nubility. Using U.S. data from large national health surveys, we show that WHR, waist/thigh, waist/stature, and BMI are all lower in the age group (15-19) in which women reach physical and sexual maturity, after which all of these anthropometric measures increase. We also show that a smaller waist, in conjunction with relatively larger hips or thighs, is strongly associated with nulligravidity and with higher blood levels of docosahexaenoic acid (DHA), a fatty acid that is probably limiting for infant brain development. Thus, a woman with the small waist and relatively large hips that men find attractive is very likely to be nubile and nulliparous, with maximal bodily stores of key reproductive resources.

Introduction

Because differential reproductive success drives adaptive evolution, selection should favor males and females whose mating preferences maximize their numbers of reproductively successful offspring. Thus both should be attracted to anthropometric traits reliably correlated with the ability of the opposite sex to contribute to this goal. In a landmark book Symons (1979) argued that the female attributes most likely to enhance male reproductive success are indicators of nubility and its associated high reproductive value (see also Andrews, Lukaszweski, Simmons, & Bleske-Rechek, 2017; Fessler et al., 2005; Marlowe, 1998; Sugiyama, 2005; Symons, 1995), and the purpose of this paper is to test whether the available evidence is consistent with Symons' view. Such a test is needed because, subsequent to Symons' formulation, a competing hypothesis proposed that men are primarily attuned to indicators of current health and fertility and that these are the female attributes indicated by the low WHRs and BMIs linked with high attractiveness (Singh, 1993a, Singh, 1993b; Tovée, Reinhardt, Emery, & Cornelissen, 1998).

The existence of male preferences for low WHRs and BMIs has been supported by many other studies in industrialized populations, where women are generally well-nourished. But any explanation of them must address why preferred values are much lower than mean or modal values in typical young women. In a recent study (Lassek & Gaulin, 2016), the mean WHR of Playboy Playmates (0.68) was 2 standard deviations below the means for typical college undergraduates (0.74) and the mean WHR (0.55) of imaginary females chosen for maximal attractiveness from comics, cartoons, animated films, graphic-novels, or video-games was 5 standard deviations below the undergraduate mean. Jessica Rabbit, the most popular imaginary female, has a WHR of 0.42. Preferred values of BMI are also in the negative tail of the actual female distribution: the mean BMI of Playmates (18.5) was 2 SD lower than the mean for college undergraduates (22.2). A recent study of 323 female comic book characters from the Marvel universe found that the mean WHR was 0.60±0.07 and the modal BMI was 17; WHR was two SD lower in 34 characters (0.61) than in the actresses portraying them in films (0.72) (Burch & Johnsen, 2019).

Singh, 1993a, Singh, 1993b suggested that men are attracted to low WHRs and BMIs because they are signs of enhanced female health and fertility, and this idea has been widely accepted (e.g., Grammer, Fink, Moller, & Manning, 2003; Marlowe, Apicella, & Reed, 2005; Pawlowski & Dunbar, 2005; Singh & Singh, 2011; Sugiyama, 2005; Tovée et al., 1998; Weeden & Sabini, 2005).

But this argument seems inconsistent with the extremity of the preferred values (above). As a result of stabilizing selection, phenotypes associated with optimal health and fertility should, and do, lie at the center—not the extreme—of the female distribution. Given such stabilizing selection on females, male preferences for traits associated with health and fertility should then target modal female values.

Based on a review of a large number of relevant studies and on new analyses, it has been recently shown that WHRs and BMIs in the negative tails of their distributions—the values rated most attractive in well-nourished populations—usually indicate poorer rather than enhanced health (Lassek & Gaulin, 2018a) and lower fertility (Lassek & Gaulin, 2018b) (although lower BMI's in younger primigravidas may reduce risks of obstructed labor and hypertension). Given that the predictions of the health-and-fertility hypothesis are not well supported, the main goal of this article is to evaluate the prior hypothesis that may better explain why males in well-nourished populations prefer female phenotypes at the negative extreme of their distributions: an evolved preference for nubility (Symons, 1979, Symons, 1995) and its demographic correlate, maximal reproductive value (Andrews et al., 2017; Fessler et al., 2005).

Despite a lack of empirical support, the health-and-fertility hypothesis has largely eclipsed Donald Symons' earlier proposal that men are attracted to nubility—to indicators of recent physical and sexual maturity in young nulligravidas (never pregnant women) (Fessler et al., 2005; Sugiyama, 2005; Symons, 1979, Symons, 1995). Symons defined the nubile phase as 3-5 years after menarche when young women are “just beginning ovulatory menstrual cycles” but have not been pregnant (Symons, 1995, p. 88). This corresponds to age 15-19 in well-nourished populations, but sexual maturity in some subsistence groups may be delayed (Ellis, 2004; Eveleth & Tanner, 1990; Symons, 1979).

Symons suggested that the female characteristics men find attractive—such as a low WHR—are indicators of nubility. And he stressed that any preference for nubility inevitably contrasts with a preference for current fertility, because the teen years of peak nubility are a well-documented period of low fertility due to a decreased frequency of ovulation, with 40-90% of cycles anovulatory, while maximum fertility is not reached until the mid to late 20's (Apter, 1980; Ashley-Montague, 1939; Ellison, Lager, & Calfee, 1987; Larsen & Yan, 2000; Loucks, 2006; Metcalf & Mackenzie, 1980; Talwar, 1965; Weinstein, Wood, Stoto, & Greenfield, 1990; Wesselink et al., 2017). Thus, if the nubility hypothesis is correct, the fertility hypothesis must be incorrect.

Nubility is closely linked to a woman's maximum reproductive value (RV), her age-specific expectation of future offspring, given the underlying fertility and mortality curves of her population (Fisher, 1930). The peak of RV is defined by survival to sexual maturity with all reproductive resources intact. The age of peak RV depends in part on the average ages of menarche and marriage, but typically ranges from 14 to 18 in human populations (Fisher, 1930; Keyfitz & Caswell, 2005; Keyfitz & Flieger, 1971). This corresponds to Symons' age of nubility. Calculations of reproductive value in the !Kung (Daly & Wilson, 1988) and in South Africa (Bowles & Posel, 2005) both found the peak age to be 15.

Symons argued that the attractiveness of the nubile age group is supported by the finding that this is the age group when marriage and first pregnancies typically occur in subsistence cultures despite reduced fecundability. For example, in the Yanomamo (polygynous hunter-horticulturalists of southern Venezuela), menarche is typically at age 12, marriage at 14, and the first birth at 16 (Symons, 1995). A similar relationship between nubility and first reproduction characterizes other subsistence populations (Table 1), where the mean age of first birth is typically under age 20 and averages 3.9±1.1 years after menarche.

In populations with access to effective contraception, the onset of sexual activity may be a better indicator of nubility than the age of marriage or first birth, although multiple factors may influence these ages. In a 2005 survey of women in 46 countries, the average age of first intercourse ranged from 15 to 19 with a mean of 17.2 (Durex, 2009) and was 17.1 in a recent sample of American women (Finer, 2007).

Prior studies suggest that attractive females exhibit the phenotypic correlates of nubility. In the Dobe !Kung, four photographed young women considered “beautiful girls” by the !Kung were all age 17 (Howell, 2000, p. 38). In samples from more developed countries, youthful bodies are also considered attractive. In a study of males viewing nude photos of female infants, children (mean age 7.7), pubescent (mean 13.5), and young adult females (mean 23.1), both viewing duration and ratings of physical attractiveness were highest for pubescent females (Quinsey, Earls, & Karamanoukian, 1996). Marlowe (1998) has suggested that an evolved attraction to nubility explains men's preference for relatively large, firm, non-sagging female breasts, and this view is supported by a study in the Hewa (Coe & Steadman, 1995).

Of particular relevance are two studies that directly explore the relationship of attractiveness to age. A recent study using body scans with raters from 10 countries found that BMI was inversely related to both rated attractiveness and to estimated age (Wang et al., 2015). In another recent study, age estimated from neck-down photographs of females in bathing suits had a strong negative relationship with attractiveness and a strong positive relationship with WHR, BMI, and especially waist/stature ratio (Andrews et al., 2017).

Symons (1995) suggests several adaptive reasons why selection might favor men preferring nubile females over older females who have higher current fertility: 1) A male who pairs with a nubile female is likely to have the maximum opportunity to sire her offspring during her subsequent most fecund years. A nubile woman is also 2) likely to have more living relatives to assist her than an older woman, and 3) to survive long enough for her children to be independent before her death. 4) A male choosing a nubile female avoids investing in children sired by other men and possible conflict with the mother (his mate) over allocation of her parental effort among his children and the children of her prior mates. By definition, a nubile woman is not investing time and energy in other men's children because she is nulliparous.

Moreover, in a wide array of competitive situations, those who stake an early claim are likely to have an advantage over those who wait until the contested resource is fully available (e.g., lining up the day before concert tickets go on sale; Roth & Xing, 1994). Thus, the men who were most strongly attracted to signs of nubility would minimize their chances of being shut out of reproductive opportunities. This dynamic would generate selection on men to seek commitment of female reproductive potential at younger ages. In such an environment, males without a preference for signs of nubility would be at a disadvantage in mating competition, and those who preferred women at the age of peak fertility (in the mid to late 20s) would likely find few available mates. In subsistence cultures, post-nubile women are very likely to be married and to have children; they are usually either pregnant or nursing and so ovulate infrequently due to ongoing reproductive commitments (Marlowe, 2005; Strassmann, 1997; Symons, 1995).

Following Symons, 1979, Symons, 1995, we consider a woman to be nubile when she has menstrual cycles, has attained maximal skeletal growth, is sexually mature based on Tanner stages (see below), but has not been pregnant. Maximal skeletal growth and stature are usually attained two to three years after the onset of menstrual periods, the latter typically occurring at ages 12-13 in well nourished populations (Eveleth & Tanner, 1990; Table 1). In a representative American sample, completed skeletal growth resulting in maximal stature was attained by age 15-16 (Hamill, Johnston, & Lemeshow, 1973).

The two widely-accepted indicators of female sexual maturity in postmenarcheal women are the attainment of 1) adult breast size and configuration of the areola and nipple, and 2) an adult pattern of pubic hair (Marshall & Tanner, 1969; Tanner, 1962). In a sample of 192 English female adolescents, the average age for attaining adult (stage 5) pubic hair was 14.4±1.1 and for adult (stage 5) breasts was 15.3±1.7. More recent samples show similar ages for attainment of breast and pubic hair maturity (Beunen, Rogol, & Malina, 2006). In other studies, puberty was judged complete by age 16-17 in American, Asian, and Swiss samples (Huang et al., 2004; Largo & Prader, 1983; Lee, 1980), based on completed skeletal growth and presence of adult secondary sexual characteristics. The timing of these developmental markers supports Symons' (1979) suggestion that nubility occurs 3 to 5 years after menarche. We will assess the timing of these developmental indicators in a large U.S. sample.

Little attractiveness research has focused on these features of the developing female phenotype, but Singh (1993b) and Symons (1995) separately suggested that both a low BMI and a low WHR are also indicators of nubility. If so, this developmental pattern would explain the male preference for low BMI and low WHR in populations where both measures increase after the nubile period.

Available evidence suggests three ways that low WHRs, BMIs, and small waists may indicate that young women in well-nourished populations are at peak nubility and reproductive value: 1) these measures are lower in the nubile age group (where nubility is defined based on completed stature growth and attainment of Tanner stage 5) than they are in older women, 2) they show that a woman is unlikely to have been pregnant, a requirement for nubility, and 3) they indicate that resources crucial for reproduction are maximal (untapped). Published evidence relevant to these points is reviewed immediately below, and we will offer new evidence that the anthropomorphic values associated with attractiveness and reproductive resources are most likely to occur in the 15-20 age group.

WHR may be a particularly good indicator of nubility because evidence suggests that it reaches a minimum during the nubile period. During female puberty, typically occurring between the ages 10-18, there is a marked increase in the amount of adipose tissue, e.g., from 12-15% to 25-26% of body weight (Boot, Bouquet, Ridder, Krenning, & Keizer-Shrama, 1997; Lim et al., 2009; Taylor, Grant, Williams, & Goulding, 2010), a percentage of body fat far greater than that seen in most other mammals, including other primates (Pitts & Bullard, 1968; Pond, 1998). Under the influence of gonadal hormones, most of this added adipose is deposited in the gluteofemoral depot (hips, buttocks, and thighs), a highly derived human trait that may have evolved to store rare fatty acids critical for the development of the large human brain (Lassek and Gaulin, 2006, Lassek and Gaulin, 2008).

This hormonally driven emphasis on gluteofemoral vs. abdominal fat stores lowers WHR, which decreases during childhood and early adolescence, reaches a minimum at ages 15 to 18, and then tends to increase (Al-Sendi, Shetty, & Musaiger, 2003; Bacopoulou, Efthymiou, Landis, Rentoumis, & Chrousos, 2015; Casey et al., 1994; de Ridder et al., 1990; de Ridder, Thijssen, Bruning, Brande, & Erich, 1992; Fredriks, Buuren, Fekkes, Verloove-Vanhorick, & Wit, 2005; Gillum, 1999; Haas, Liepold, & Schwandt, 2011; Kelishadi et al., 2007; Martinez, Devesa, Bacallao, & Amador, 1994; Moreno et al., 2007; Taylor et al., 2010; Westrate, Deurenberg, & Tintern, 1989). This developmental pattern supports the idea that a low WHR is a relatively conspicuous marker of nubility (in addition to other signs of sexual maturity which may be less readily assessable, such as menstruation, breast and pubic-hair development, and attainment of maximal stature).

In well-nourished populations BMIs are also lower in nubile adolescents than in older women. In a longitudinal study of American women that began in the 1930's, the mean BMI increased from 16.7 kg/m² in early adolescence to 18.9 in late adolescence, 22.1 at age 30, 24.1 at age 40, and 26.1 at age 50 (Casey et al., 1994). Cross-sectional female samples show parallel age-related weight increases (highly correlated with BMI) (Abraham, Johnson, & Najjar, 1979; Burke et al., 1996; Schutz, Kaye, & Pichard, 2002; Stoudt, Damon, McFarland, & Roberts, 1965). Controlling for social class and parity, age was a significant predictor of BMI in a large United Kingdom sample (Gulliford, Rona, & Chinn, 1992). In a study in which males estimated the age of female figures varying in BMI and WHR (Singh, 1995), they judged the figures with the lowest BMIs (15) to be the youngest, with an estimated age of 17-19. We will explore the relationship of WHR and BMI with age in a large American sample.

However, in contrast to women in well-nourished groups, in subsistence populations women's BMIs may peak at the age of nubility and subsequently decrease with age and parity (see Lassek & Gaulin, 2006). Notably, men in such populations often prefer the higher BMIs which in these cultures indicate nubility (Sherry & Marlowe, 2007; Sugiyama, 2005; Yu & Shepard, 1998). Thus, a consistent preference for the BMIs most strongly associated with nubility could explain an apparent cross-cultural inconsistency in body-shape preferences, which is difficult to explain using the health-and-fertility hypothesis.

An essential part of Symons, 1979, Symons, 1995 definition of nubility (and the high reproductive value it represents) is the lack of any previous pregnancy (i.e., nulligravidity); nubile women have attained physical and sexual maturity without yet expending any reproductive potential. Prior evidence suggests that a low WHR (or small waist size) is also a strong indicator of nulliparity (Bjorkelund, Lissner, Andersson, Lapidus, & Bengtsson, 1996; Gunderson et al., 2009, Gunderson et al., 2008; Gunderson, Murtaugh, Lewis, & West, 2004; Lanska, Lanska, Hartz, & Rimm, 1985; Lassek & Gaulin, 2006; Lewis et al., 1994; Luoto, Mannisto, & Raitanen, 2011; Mansour, Ajeel, & Ajeel, 2009; Rodrigues & Da Costa, 2001; Smith et al., 1994; Tonkelaar et al., 1989; Wells et al., 2010). Similarly, a recent study (Butovskaya et al., 2017) found a strong positive relationship between WHR and parity in seven traditional societies.

Like WHR, BMI also increases with parity in well nourished populations (Abrams, Heggeseth, Rehkopf, & Davis, 2013; Bastian, West, Corcoran, & Munger, 2005; Bobrow, Quigley, Green, Reeves, & Beral, 2013; Koch et al., 2008; Nenko, Jasienska, Nenko, & Jasienska, 2009; Rodrigues & Da Costa, 2001). Some studies have suggested that BMI may be more strongly related to parity than it is to age (Koch et al., 2008; Nenko et al., 2009), although this may be less true in older women (Trikudanathan et al., 2013). We will explore the relationships of WHR and BMI to age and parity in a large American sample.

In two studies of men's perceptions, higher WHRs were judged to strongly increase the likelihood of a previous pregnancy (Andrews et al., 2017; Furnham & Reeves, 2006). Thus, anthropometric data suggest that a low WHR and BMI may indicate nulliparity, as well as a young age, and psychological data suggest that men interpret these female features as carrying this information.

Because they have reached sexual maturity but have not yet been pregnant, nubile women should have maximum supplies of reproductive resources that are depleted by pregnancy and nursing, such as the omega-3 fatty acid docosahexaenoic acid (DHA). Many studies have shown that DHA is an important resource supporting neuro-cognitive development in infants and children (Janssen & Kiliaan, 2014; Joffre, Nadjar, Lebbadi, Calon, & Laye, 2014; Lassek and Gaulin, 2014, Lassek and Gaulin, 2015), and DHA stored in adipose is depleted by successive pregnancies (Dutta-Roy, 2000; Hanebutt, Demmelmair, Schiessl, Larque, & Koletzko, 2008; Hornstra, 2000; Lassek and Gaulin, 2006, Lassek and Gaulin, 2008; Min et al., 2000). Stores of DHA would likely have been an increasingly important aspect of mate value in the hominin lineage as it experienced dramatic brain expansion.

Most of the DHA used for fetal and infant brain development is stored in gluteofemoral fat until it is mobilized from this depot during pregnancy and nursing (Lassek & Gaulin, 2006; Rebuffe-Scrive, 1987; Rebuffe-Scrive et al., 1985). Indeed, a low WHR is associated with higher circulating levels of DHA (Harris et al., 2012; Karlsson et al., 2006; Micallef, Munro, Phang, & Garg, 2009; Wang et al., 2008), as is a smaller waist size and lower levels of abdominal fat (Alsharari et al., 2017; Bender et al., 2014; Howe et al., 2014; Karlsson et al., 2006; Wagner et al., 2015).

Thus, young women with smaller waists and WHRs are likely to have higher levels of DHA in their stored fat and so can provide more DHA to their children during pregnancy and nursing which may result in enhanced cognitive ability in their offspring. Consistent with the possibility that female body shape reveals stored neuro-cognitive resources, in a large sample of American mothers those with lower WHRs had children who scored higher on cognitive tests (controlling for other relevant factors, including income and education variables) (Lassek & Gaulin, 2008). Moreover, the children of teenage mothers, at particular risk for cognitive deficits, scored significantly better on cognitive tests when their mothers had lower WHRs. To further examine the reproductive role of the gluteofemoral depot, we will assess the relationship of the waist/thigh ratio to plasma levels of DHA.

Hypothesis: In well-nourished populations, women with low WHRs and low BMIs are judged attractive because these low values coincide with attainment of completed growth and sexual maturity, indicate nulligravidity, and indicate maximal stores of fatty acids critical for infant brain development.

Prediction 1

In a large sample of American women, WHR, waist/stature ratio, waist/thigh ratio, and BMI will a) exhibit lower values (compared to older women) around the ages of physical and sexual maturity, and b) be significantly lower in nulligravid compared to pregnant or parous women.

Prediction 2

Women with lower waist/stature and waist/thigh ratios will have a higher percentage of DHA in their plasma fatty acids.