Ill

Narrow Broad Broad waist, waist, waist, small large small breasts breasts breasts

Figure 7.14 Relationships between waist size, breast size, and mid-cycle levels of salivary oestradiol in women. Women with narrow waists and large breasts have the highest oestrogen levels.

Source: From Jasienska et al. (2004).

Members of the genus Homo, which preceded H. sapiens in Africa, had a very similar post-cranial anatomy, walked upright, and were probably subject to thermoregulatory or other selective pressures which resulted in reduction of body hair (Wheeler 1984; Rantala 2007). It is entirely possible, therefore, that H. ergaster or H. erectus females would have possessed narrower waists, fatter buttocks and thighs, and larger breasts than males. The males, by contrast, were likely to have been significantly taller, more muscular and physically stronger than the females. There are compelling reasons to suggest that these traits did not arise de novo in H. sapiens, and that sexual selection had affected body shape and composition in both the sexes prior to the advent of anatomically modern humans.

Sex differences in skin colour

Darwin (1871) noted the tendency for women in various parts of the world to have lighter skin than men. As an example, he cited Schweinfurth concerning the Monbuttoos of Africa: 'Like all her race she had a skin several shades lighter than her husband's, being something of the colour of half-roasted coffee.' Darwin also suggested that sex differences in skin colour might have been influenced by sexual selection during human evolution. Hormonal changes at puberty are now known to effect the expression of this sex difference. Thus, in young women, oestrogen promotes lightening of the skin, whilst in young men increased androgen secretion favours a darker complexion. This is due both to the deposition of melanin in the epidermis and the greater increases in red blood cells (and haemoglobin levels) in deeper layers of the skin, resulting in 'browner and ruddier complexions' in men than in women (Frost 1994).

Skin colour varies a great deal between human populations. Darker pigmentation, such as occurs in modern African populations, is most likely to represent the ancestral condition of H. sapiens. The layer of melanin in the epidermis helps to protect the skin against harmful effects of ultraviolet radiation, as the sun is especially powerful in equatorial regions. Protection against sunburn would obviously have been important for human ancestors in Africa. It is interesting that babies may initially be quite light-skinned in some African populations, but then the skin darkens rapidly in the days following birth. Natural selection may have favoured such rapid deposition of melanin in infants as a protection against sunburn. The emigration of H. sapiens from Africa to more-northerly latitudes, such as occurred when modern humans reached Europe approximately 40,000 years ago, was associated with the loss of melanin and the evolution of lighter skin. This may have been adaptive in maximizing the ability of the skin to synthesize vitamin D, under conditions of low ultraviolet exposure (Jablonski and Chaplin 2000; Jablonski 2006). It has also been suggested that lighter-skinned people may fare better than those who are dark-skinned in extremely cold conditions, such as those which pertained in northern Europe during the ice-ages of the Palaeolithic era (Post, Daniels, and Binford 1975).

Sexual dimorphism in skin tone has been reported in a large number of ethnic groups worldwide; the differences are subtle in many cases but they appear to be consistent, with women having slightly lighter skin than men (Frost 1988). Skin colour may provide a visual cue to female health, age, and reproductive condition. Although the female skin lightens due to oestrogenic effects with the onset of physical maturity (Tanner 1978), subsequent pregnancies and periods of lactation often bring about localized changes in pigmentation. These may affect the

waist, large breasts

skin of the face, breasts, and abdomen, producing lasting changes and visible signs of aging (Wong and Ellis 1984; Sodhi and Sausker 1988). Symons (1995) has suggested that masculine preferences for lighter female skin tones might have undergone sexual selection, because such preferences would have enhanced the reproductive success of the men concerned. The skin, free of its covering of hair, becomes a canvas on which visual cues of health and reproductive condition may be displayed. Ethnographic comparisons confirm that male preferences for lighter skin in women exist in various human populations (van den Berghe and Frost 1986). As an example of recent work on this question, Figure 7.15 shows the results of studies carried out in Africa, New Zealand, China, and USA to examine male preferences for female skin colour. In each case, men were asked to choose which of five, back-posed female images they found most sexually attractive. The five images were identical except for skin colour. One image represented the colour typical for the culture being studied; two images were made progressively lighter in skin tone and two were darker. A computerized technique was used to control exactly the degree to which images were lighter or darker than usual (Dixson et al. 2007a; 2007b; in press). The results provide some support for the hypothesis that lighter female skin colours are more attractive to men, but they are not conclusive. Thus, in China, the lightest skin colour was clearly the most attractive, followed by the slightly lighter than average skin tone. Average and darker skin colours were rated as much less attractive by Chinese men (Figure 7.15). In both New Zealand and USA (California), darkening of the skin also rendered female figures less attractive, but only in California was lighter skin (one shade above average) rated as significantly more attractive. In the African (Cameroonian) sample, none of the five female images was rated as more attractive than would be expected by chance alone. The results of these studies are promising, but they should be extended to include other populations before conclusions can be drawn about the role of sexual selection in the evolution of human skin colour. In particular, it would be important to determine whether men are responsive to the subtle sex differences in skin colour which occur naturally in human populations.

The images used in computerized questionnaires represent more pronounced variations in female skin tone than are typical of natural populations. Computerized images may represent supernormal stimuli (to borrow a term from ethology) in the same way that depictions of excessively slim female waists, or large breasts, might exaggerate features which men find attractive.

Sexual dimorphism of the human face

Hormonal changes during puberty and adolescence also affect growth and sexual dimorphism of craniofacial traits in human beings. Men tend to develop a larger jaw, chin, and cheekbones, a somewhat heavier brow-ridge and narrower, deeper-set eyes than women. These facial changes, which emerge gradually from puberty onwards in young men, reflect in part the effects of higher levels of testosterone. In young women, by contrast, a higher level of oestrogen, coupled with a much lower tendency to secrete testosterone, favours continued growth of more juvenile facial traits; a smaller chin and brow, larger eyes in relation to the size of the face and, often, fuller lips. As discussed above, the skin also exhibits differences between the sexes, so that the female complexion tends to lighten under the action of oestrogen. In men, testosterone stimulates the development of a darker complexion, as well as the growth of facial hair; this last trait will be considered in the next section.

Among the anthropoid primates, facial communication plays an integral role in many aspects of social and sexual behaviour (Van Hooff 1967; Dixson 1998a). Human non-verbal communication is complex, and we employ a rich repertoire of facial displays, many of which developed in ancestral forms prior to the evolution of language. H. sapiens is the only primate species in which the sclera of the eye is white, rather than being pigmented. This makes the iris and pupil of the human eye stand out in contrast to the surrounding 'white' of the eye. Judgments of gaze direction and eye-contact are most important during facial communication (Conway et al. 2008), so that these functions may be facilitated by the white sclera of the human eye (Kobayashi and Kohshima 2001). Facial cues are likely to play a fundamental role in human assessments of sexual attractiveness and in mate choice. Cross-cultural studies have shown that facial

China

China

Cameroon

Lighter —- Average -Darker

Female skin colour

Figure 7.15 Results of cross-cultural studies to examine men's preferences for female skin colour. Data show the numbers of men who rated each of six female images as most attractive. The images differed only in their skin tone. The dashed line indicates the numbers of men who would be expected to select each image by chance alone. **P < .01; ***P < .001 (%2 tests). Source: Data are from Dixson et al. (2007a; 2007b; in press).

expressions reflecting certain fundamental emotions, such as joy, anger, surprise, and fear, are universal in H. sapiens (Ekman and Friesen 1971; Ekman 1973). That the human proclivity to exhibit such expressions is genetically determined is indicated by the finding that individuals who have been blind from birth show them, and even display distinctive familial traits of facial expression (Peleg et al. 2006). We should expect, therefore, that sexually dimorphic traits of the human face, whether in repose or when used for subtle non-verbal displays between the sexes, might be highly significant in assessing another individual's motivation and personality, as well as their health and attractiveness. A considerable volume of research has sought to define those qualities of the human face which determine beauty and attractiveness to the opposite sex. The roles of averageness and of symmetry have been mooted to be of importance in this regard (e.g. reviews by Penton-Voak and Perrett 2000; Rhodes 2006). The notion that average-ness in human faces might be most attractive (Lan-glois and Roggman 1990) is based upon the finding that composite faces, formed by blending images of a number of subjects, are often considered beautiful. However, a careful study of this problem led Perrett, May, and Yoshikawa (1994) to conclude that subjects (in UK and Japan) find composites of the most attractive faces in a selection of images to be more attractive than the overall average for this larger set of images. They propose that certain fundamental determinants of facial attractiveness may be shared across cultures and that preferences for these traits might represent 'a directional selection pressure on the evolution of human face shape'. Facial symmetry might be an example of such a cross-culturally robust cue, as it is a signal of genetic quality and developmental stability. As an example, Little, Api-cella, and Marlowe (2007) have shown that Hadza hunter-gatherers show preferences for facial symmetry that are more pronounced than those of people in the UK. In Figure 7.16, the reader may observe the very subtle changes required to produce symmetrical faces and also the degree of sexual dimorphism displayed by Hadza faces.

Here I am concerned primarily with the question of whether sexually dimorphic human facial traits might influence attractiveness and mate choice in men and women. If consistent effects can be identified, can these preferences tell us anything about the origins and evolution of sexual behaviour in the genus Homo? There is increasing evidence to support the view that, like the WHR, the female face provides visual signals of underlying health and fertility (Johnston and Franklin 1993; Perrett et al. 1994, 1998). Law-Smith et al. (2006) have demonstrated a positive correlation between circulating levels of oestrogen during the follicular phase of the menstrual cycle and ratings of women's faces for femininity, attractiveness, and health (Figure 7.17). Thus, women who have higher oestrogen levels are consistently rated as having more attractive (and healthy) faces. The reader may examine in Figure 7.17 the composite faces produced by Law-Smith et al; in my own experience of showing these to some hundreds of young men and women, they overwhelmingly rate the higher-oestrogen composite as more attractive in the absence of any prior information about possible differences between the photographs. It is evident that these composite faces differ subtly in a number of aspects of morphology; there are possible differences in complexion to consider as well. Indeed, there is some evidence that photographs of women's faces taken during the follicular phase of the menstrual cycle are rated as more attractive than photographs of the same individuals during the luteal phase (Roberts et al. 2004). There is the possibility, therefore, that women's facial attractiveness might convey information about short-term as well as longer-term cues to reproductive status and health.

The situation is more complex where masculine facial traits, health, hormonal status and attractiveness are concerned. Testosterone affects the degree to which male facial traits develop during puberty and adolescence, and there is evidence that more masculinized faces are perceived as more dominant, but not necessarily as more attractive, by women (Swaddle and Reierson 2002). Male teenagers with more dominant, masculinized facial traits report coital activity at younger ages than others (Mazur, Halpern, and Udry 1994). In a study of military officers who were graduates of the West Point Military Academy in the USA, dominant facial appearance was a reliable predictor of the ranks ultimately attained by men (Mueller and Mazur 1997). Those who became generals also had more children; an

I 58

European

Hadza

Figure 7.16 Symmetrical (ai and aii) and unaltered (bi and bii) photographs of the faces of a Hadza woman and man. The Hadza hunter-gatherers of Tanzania show greater preferences for facial symmetry than is the case for people tested in the UK.

Source: From Little, Apicella, and Marlowe (2007).

Figure 7.17 Which face is most attractive? Both photographs are composite images of a number of women. On the left, is a composite of faces of women who have high follicular phase levels of oestradiol 17p. The right hand composite image is of women who have lower oestrogen levels.

Source: After Law-Smith et al. (2006).

average of 3.67 vs. 3.02 for other officers (P < .001). Yet it is not the case that women always find masculinized faces more attractive; preferences for larger jaws and cheekbones in male faces have been reported in some studies (Grammer and Thornhill 1994; Scheib, Gangestad, and Thornhill 1999), whilst Perrett et al. (1998) found that women preferred more 'feminized' or 'baby-faced' males. As discussed in the last chapter, women's hormonal status can affect their judgments of the attractiveness of a variety of masculine traits, including more masculinized faces, which receive higher attractiveness ratings during the fertile phase of the menstrual cycle (Penton-Voak et al. 1999; Penton-Voak and Perrett 2000).

Women's preferences for facial masculinity may be predicted from their ratings of their own partner's masculinity and from stated preferences in a theoretical 'ideal partner' (DeBruine et al. 2006). Women who are facially very attractive and who have a low WHR are more likely to prefer more masculine faces (Penton-Voak et al. 2003). Rapidity of sexual development also affects female preferences; women who have intercourse at younger ages tend to prefer masculinized faces (Cornwell et al. 2006).

It is possible that such results may reflect different female strategies in relation to qualities signalled by masculine facial traits. Thus a highly masculine face may signal health and greater ability to withstand the immunosuppressive effects of testosterone (Rhodes et al. 2003). This line of reasoning is based upon Folstad and Karter's (1992) immunocompetence-handicap hypothesis, developed on the basis of animal studies and supported by research which demonstrates a correlation between masculine secondary sexual traits and immune function in various species (M0ller, Christe, and Lux 1999). Well-developed masculine facial cues may also be reflective of other physical and behavioural qualities which are attractive to women. It has even been reported by Soler et al. (2003) that facial attractiveness in men correlates with measurements of semen quality, such as sperm motility and morphology. Although these correlations were not highly significant (P < .05), they are consistent with the results of experiments showing that masculine secondary sexual traits are positively correlated with semen quality in animals (e.g. in zebra finches: Birkhead and Fletcher 1995; red deer stags: Malo et al. 2005). Yet, if men's health, strength, and reproductive potential are reflected by facial masculinization, it is surprising that some women prefer more feminized faces (Perrett et al. 1998). In discussing this quandary Penton-Voak and Perrett (2000) point out that highly masculinized faces may also 'elicit negative personality attributions; coldness, dominance and dishonesty, for example'. Given the importance of personality assessments in human mate choice (Buss 1989), there may be advantages for women in choosing men whom they believe are likely to invest more in relationships and care of offspring. Roney et al. (2006) reported that women rated the images of men with more masculinized faces (and higher salivary testosterone levels) as more physically attractive, but assessed men with softer facial features as being more interested in children and more desirable for long-term relationships. One current limitation of all these studies is the paucity of cross-cultural data on human facial traits and attractiveness. With the exception of work on the Hadza, almost all studies have been conducted on populations in the USA, UK, and Japan.

The degree of sexual dimorphism in human facial traits is not as extreme as that which occurs in many non-human primates. Species that are highly sexually dimorphic in body size due to effects of sexual selection, such as gorillas, proboscis monkeys, golden monkeys, hamadryas baboons, orangutans, and mandrills, are often characterized by the possession of striking masculine secondary sexual adornments of the head and face. In none of these monkeys and apes do males invest as heavily in offspring and show the same degree of paternal care as is typical of H. sapiens. Evidence acquired from studies of facial attractiveness and mate choice in human beings supports the view that facial traits have undergone sexual selection in both the sexes. There may have been selective forces constraining the development of masculine facial cues, however, so that men's faces are not necessarily rendered more attractive by over-emphasis of traits such as heavy jaws and brow ridges. A striking sexually dimorphic trait which is stimulated by testosterone in men concerns growth of facial hair. The evolutionary significance of the human beard is discussed in the next section. It is also relevant to note that those non-human primates which are monogamous and which form long-term family groups tend to be sexually monomorphic as regards their facial traits. Examples include many marmosets and tamarins, the titi monkeys and owl monkeys of the New World, as well as most of the smaller apes (gibbons) of Southeast Asia. There are exceptions, however, such as the white-faced saki (Pithecia pithecia) of South America, in which the striking white facial colouration occurs only in males.

Human beings display the morphological characteristics of a species in which sexual selection has influenced the evolution of facial traits more than would be expected in a primarily monogamous primate. This again hints at the likely occurrence of polygyny as well as monogamy in human precursors. The final section of this chapter examines, in greater detail, the relationships between the degree of development of masculine secondary sexual visual traits and mating systems in monkeys, apes, and human beings.

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