Wednesday, May 8, 2019

The women men are attracted to in well-nourished populations have low body mass indices & small waist sizes combined with relatively large hips; men are attracted to signs of being nubile & nulliparous

Evidence supporting nubility and reproductive value as the key to human female physical attractiveness. William D. Lassek, Steven J. C. Gaulin. Evolution and Human Behavior, May 8 2019. https://doi.org/10.1016/j.evolhumbehav.2019.05.001

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.

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Introduction
Because differential reproductive success drives adaptive evolution, selection should favor males and females whose mating preferences maximize their numbers of reproductively successful offspring. Thusboth should be attracted to anthropometric traits reliably correlated with the ability of the opposite sex to contribute to this goal. In a landmark bookSymons (1979) argued that the female attributesmost likely to enhance male reproductive success are indicators of nubility and its associated high reproductive value (see also Andrews et al.,2017; Fessleret al, 2005; Marlowe, 1998; Sugiyama, 2005; Symons,1995), and the purpose of this paper is to test whether the availableevidence isconsistent with Symons’view. Such a test is needed because, subsequentto Symons’formulation,a competing hypothesis proposed that men are primarily attuned to indicators of current health and fertilityand that these are the female attributes indicated bythe low WHRs and BMIslinked with high attractiveness(Singh, 1993a; 1993b; Tovée et al., 1998). Theexistence of male preferences for low WHRs and BMIs hasbeen supported by many other studies in industrialized populations,where women are generally well-nourished.Butanyexplanation ofthemmust address whypreferred values are much lower than mean or modal values in typical young women. In a recent study (Lassek&Gaulin, 2016), the mean WHR of PlayboyPlaymates (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, animatedfilms, 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 323female comic book characters from the Marvel universefound 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 actressesportraying themin films (0.72)(Burch & Johnsen, 2019).

1.1 Health and fertility as the basis for female attractiveness?

Singh (1993a, 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., Grammeret al.,2003; Marloweet al.,2005; Pawlowski&Dunbar,2005; Singh &Singh 2011; Sugiyama, 2005; Tovée et al.,1998; Weeden & Sabini,2005). But thisargument 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 selectionon 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 thatWHRs and BMIs in the negative tails of their distributions—the values rated most attractive in well-nourished populations—usually indicate poorerrather than enhanced health (Lassek&Gaulin,2018a) and lowerfertility (Lassek&Gaulin,2018b)(although lower BMI’sin younger primigravidasmay reduce risksof 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 theprior hypothesis that maybetter explain why males in well-nourished populations prefer female phenotypes at the negative extreme of their distributions: an evolvedpreference for nubility (Symons 1979, 1995) and its demographic correlate, maximal reproductive value (Andrews et al.,2017; Fessler et al., 2005).

1.2 Nubility as the basis for female attractiveness?
Despite a lack of empirical support, the health-and-fertility hypothesis has largely eclipsed Donald Symons’s earlier proposal thatmen are attracted to nubility—to indicators of recent physical and sexual maturity in young nulligravidas (never pregnant women) (Fessler et al., 2005; Symons,1979;1995; Sugiyama, 2005). Symons defined the nubile phase as 3-5 years after menarche when young women are “just beginning ovulatorymenstrual cycles” but have not been pregnant (Symons.1995, p. 88). This corresponds to age 15-19 in well-nourished populations, but sexual maturityin some subsistence groupsmay be delayed (Ellis,2004; Eveleth&Tanner,1990; Symons 1979). Symons suggested that the female characteristics men find attractive—such as a low WHR—are indicatorsof nubility. And he stressedthat 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 lowfertilitydue 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; Ellisonet al., 1987; Larsen&Yan,2000; Loucks,2006; Metcalf&Mackenzie,1980; Talwar, 1965; Weinsteinet al., 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 14to 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 & Wilson, 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 groupwhen marriage and first pregnancies typically occur in subsistence culturesdespite 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). Asimilar relationship between nubility and first reproduction characterizesother subsistence populations(Table 1), wherethe mean age of first birth is typically under age 20 and averages 3.9±1.1years after menarche.Inpopulationswith access toeffectivecontraception,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 samplesfrom 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 (Quinseyet al., 1996). Marlowe(1998) has suggested thatan evolved attractionto 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 preferringnubile 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 siredby 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 sheis 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 ticketsgo 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 offemale 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; Strassman, 1997;Symons,1995).

1.3 External signs of nubility
Following Symons (1979;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 beenpregnant. 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 et al., 1973). The two widely-accepted indicators of female sexual maturity in postmenarcheal women are the attainment of 1)adult breast sizeandconfiguration of the areola and nipple, and 2) an adult pattern of pubic hair (Tanner,1962, Marshall&Tanner,1969). 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 (Beunenet al., 2006). In other studies, puberty was judged complete by age 16-17 in American, Asian, and Swiss samples (Huanget al., 2004;Largo&Prader,1983;Leeet al., 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 assessthe timing of these developmental indicators in a large U.S. sample.

Little attractiveness research has focused on these features of the developing female phenotype, butSingh (1993b) and Symons (1995) separately suggested that both a low BMIand 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 threeways 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 measuresare lower in the nubile age group (where nubility is defined based on completed stature growth and attainment of Tanner stage5) 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 newevidence that the anthropomorphic values associated with attractiveness and reproductive resources are most likely to occur in the 15-20 age group.

1.3.1 Low WHR and BMI as indicatorsof attainment of sexual maturity
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 occurringbetween theages 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 et al., 1997, Lim et al., 2009; Taylor et al., 2010), a percentage of body fat far greater than that seen in most other mammals, including other primates (Pond, 1998; Pitts&Bullard, 1968). Under the influence of gonadal hormones, mostof this added adipose is deposited in the gluteofemoral depot (hips, buttocks, and thighs), a highly derived human traitthat may haveevolved to store rare fatty acids critical for the development of the large human brain (Lassek &Gaulin, 2006; 2007;2008). Thishormonally driven emphasis on gluteofemoral vs. abdominal fatstores lowers WHR, which decreases during childhood and early adolescence, reaches a minimum at ages 15 to 18, and then tends to increase (Al-Sendi et al., 2003; Bacopoulou et al., 2015; Casey et al., 1994; de Ridder et al., 1990;1992; Fredriks et al., 2005; Gillum,1999; Haas et al., 2011; Kelishadi et al., 2007; Martinez et al., 1994; Moreno et al., 2007; Taylor et al., 2010; Westrate et al., 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 andpubic-hair development, and attainment of maximal stature).In well-nourished populationsBMIs 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/m2in 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 et al., 1979;Burke et al., 1996; Schutz et al., 2002; Stoudt et al., 1965). Controlling for social class and parity, age was a significant predictor of BMI in a large United Kingdom sample (Gulliford et al., 1992). In a study in which males estimated the age of femalefigures 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 decreasewith 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.

1.3.2 Low WHRs and BMIs and smaller waist sizes indicate a lower likelihood of previous pregnancy
An essential part of Symons’ (1979, 1995) definition of nubility (and the high reproductive value it represents) is the lack of any previous pregnancy(i.e., nulligravidity); nubile womenhaveattained physical and sexual maturity without yet expending any reproductive potential.Priorevidence suggests that a low WHR (or small waist size) is also a strong indicator of nulliparity (Bjorkelund et al., 1996; Gunderson et al., 2004; 2008; 2009; Lanska et al., 1985; Lassek &Gaulin,2006; Lewis et al., 1994; Luoto et al., 2011; Mansour et al., 2009; Rodrigues &Da Costa,2001; Smith et al., 1994; Tonkelaar et al., 1989; Wells et al., 2010). Similarly, a recent study (Butovskya et al., 2017) found a strong positive relationship between WHR and parity in seven traditional societies. Like WHR, BMI also increases with parity in wellnourished populations (Abrams et al., 2013; Bastianet al., 2005;Bobrowet al., 2013; Rodrigues &Da Costa,2001 Kochet al., 2008; Nenkoet al., 2009). 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 inolder women (Trikudanathanet 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 (Andrewset 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.

1.4 Smaller WHRs and waist sizes indicate greater availability of reproductive resources
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 ininfants and children(Janssen & Killiaan, 2014; Joffre et al., 2014; Lassek &Gaulin,2014;2015), andDHA stored in adiposeisdepleted by successive pregnancies (Dutta-Roy,2000, Hanebutt et al., 2008; Hornstra,2000; Lassek &Gaulin,2006;2008; Min et al., 2000). Stores of DHA would likely have beenan increasingly important aspect of mate value in the homininlineage as itexperienced dramatic brain expansion.Most of the DHA used for fetal and infant brain development is stored in gluteofemoralfatuntil it is mobilized from this depot during pregnancy and nursing(Lassek &Gaulin, 2006; Rebuffe-Scrive et al., 1985;1987). Indeed,a low WHR is associated with higher circulating levels of DHA (Harris et al., 2012; Karlsson et al., 2006; Micallef et al., 2009; Wang et al., 2008), as isa smaller waist size and lower levels ofabdominal fat(Alsahari 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 thepossibilitythat 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 ofteenage mothers, at particular risk for cognitive deficits, scoredsignificantly 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.

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