Does attractiveness in men provide clues to semen quality?

The psychological mechanisms underlying attractiveness judgements in humans are thought to be evolved adaptations for finding a high quality mate. The phenotype-linked fertility hypothesis proposes that females obtain reliable information on male fertility from male expression of sexual traits. A previous study of Spanish men reported that facial attractiveness was positively associated with semen quality. We aimed to determine whether this effect was widespread by examining a large sample of Australian men. We also extended our study to determine whether cues to semen quality are provided by components of attractiveness: masculinity, averageness and symmetry. Each male participant was photographed and provided a semen sample that was analyzed for sperm morphology, motility and concentration. Two independent sets of women rated the male photographs for attractiveness, and three further sets of 12 women rated the photographs for masculinity, symmetry or averageness. We found no significant correlations between semen quality parameters and attractiveness or attractive traits. Although male physical attractiveness may signal aspects of mate quality, our results suggest that phenotype-linked cues to male fertility may not be general across human populations.     

Does Masculinity Matter? The Contribution of Masculine Face Shape to Male Attractiveness in Humans

Background

In many animals, exaggerated sex-typical male traits are preferred by females, and may be a signal of both past and current disease resistance. The proposal that the same is true in humans – i.e., that masculine men are immunocompetent and attractive – underpins a large literature on facial masculinity preferences. Recently, theoretical models have suggested that current condition may be a better index of mate value than past immunocompetence. This is particularly likely in populations where pathogenic fluctuation is fast relative to host life history. As life history is slow in humans, there is reason to expect that, among humans, condition-dependent traits might contribute more to attractiveness than relatively stable traits such as masculinity. To date, however, there has been little rigorous assessment of whether, in the presence of variation in other cues, masculinity predicts attractiveness or not.

Methodology/Principal Findings

The relationship between masculinity and attractiveness was assessed in two samples of male faces. Most previous research has assessed masculinity either with subjective ratings or with simple anatomical measures. Here, we used geometric morphometric techniques to assess facial masculinity, generating a morphological masculinity measure based on a discriminant function that correctly classified >96% faces as male or female. When assessed using this measure, there was no relationship between morphological masculinity and rated attractiveness. In contrast, skin colour – a fluctuating, condition-dependent cue – was a significant predictor of attractiveness.

Conclusions/Significance

These findings suggest that facial morphological masculinity may contribute less to men''s attractiveness than previously assumed. Our results are consistent with the hypothesis that current condition is more relevant to male mate value than past disease resistance, and hence that temporally fluctuating traits (such as colour) contribute more to male attractiveness than stable cues of sexual dimorphism.     

The masculinity paradox: facial masculinity and beardedness interact to determine women's ratings of men's facial attractiveness

In many species, male secondary sexual traits have evolved via female choice as they confer indirect (i.e. genetic) benefits or direct benefits such as enhanced fertility or survival. In humans, the role of men's characteristically masculine androgen‐dependent facial traits in determining men's attractiveness has presented an enduring paradox in studies of human mate preferences. Male‐typical facial features such as a pronounced brow ridge and a more robust jawline may signal underlying health, whereas beards may signal men's age and masculine social dominance. However, masculine faces are judged as more attractive for short‐term relationships over less masculine faces, whereas beards are judged as more attractive than clean‐shaven faces for long‐term relationships. Why such divergent effects occur between preferences for two sexually dimorphic traits remains unresolved. In this study, we used computer graphic manipulation to morph male faces varying in facial hair from clean‐shaven, light stubble, heavy stubble and full beards to appear more (+25% and +50%) or less (?25% and ?50%) masculine. Women (N = 8520) were assigned to treatments wherein they rated these stimuli for physical attractiveness in general, for a short‐term liaison or a long‐term relationship. Results showed a significant interaction between beardedness and masculinity on attractiveness ratings. Masculinized and, to an even greater extent, feminized faces were less attractive than unmanipulated faces when all were clean‐shaven, and stubble and beards dampened the polarizing effects of extreme masculinity and femininity. Relationship context also had effects on ratings, with facial hair enhancing long‐term, and not short‐term, attractiveness. Effects of facial masculinization appear to have been due to small differences in the relative attractiveness of each masculinity level under the three treatment conditions and not to any change in the order of their attractiveness. Our findings suggest that beardedness may be attractive when judging long‐term relationships as a signal of intrasexual formidability and the potential to provide direct benefits to females. More generally, our results hint at a divergence of signalling function, which may result in a subtle trade‐off in women's preferences, for two highly sexually dimorphic androgen‐dependent facial traits.     

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.     

Cross-cultural effects of color,but not morphological masculinity,on perceived attractiveness of men's faces

Much attractiveness research has focused on face shape. The role of masculinity (which for adults is thought to be a relatively stable shape cue to developmental testosterone levels) in male facial attractiveness has been examined, with mixed results. Recent work on the perception of skin color (a more variable cue to current health status) indicates that increased skin redness, yellowness, and lightness enhance apparent health. It has been suggested that stable cues such as masculinity may be less important to attractiveness judgments than short-term, more variable health cues. We examined associations between male facial attractiveness, masculinity, and skin color in African and Caucasian populations. Masculinity was not found to be associated with attractiveness in either ethnic group. However, skin color was found to be an important predictor of attractiveness judgments, particularly for own-ethnicity faces. Our results suggest that more plastic health cues, such as skin color, are more important than developmental cues such as masculinity. Further, unfamiliarity with natural skin color variation in other ethnic groups may limit observers' ability to utilize these color cues.     

The relationship between sexual dimorphism in human faces and fluctuating asymmetry

Previous studies have found both support and lack of support for a positive relationship between masculinity and symmetry, two putative signs of mate quality, in male faces. We re-examined this relationship using an explicit measure of facial fluctuating asymmetry, as well as other measures of asymmetry, and measures of facial masculinity/femininity. We also used ratings of these traits for faces. Further, we examined the relationship between facial sexual dimorphism and body asymmetry. We found no significant correlations between facial masculinity and any of our measures of asymmetry or ratings of symmetry in males. Facial femininity was not consistently associated with facial symmetry in females, but was associated with body symmetry. Therefore, for females, but not males, facial femininity and body symmetry may reflect similar aspects of mate quality. We also examined the relationships between trait ratings and measurements. Our results provide validation of our ability to measure aspects of asymmetry that are perceived to be symmetrical, and aspects of sexual dimorphism that are perceived as feminine in females and masculine in males.     

Vocal and Facial Attractiveness Judgments of Children, Adolescents and Adults: the Ontogeny of Mate Choice

Physical traits are thought to be used as indicators of mate quality, allowing individuals to select mates most likely to help them bear the fittest offspring. As the capacity for human sexual behaviour emerges at puberty, we investigated whether adult‐like judgments of the relative attractiveness of opposite‐sex individuals also arise at puberty. Following previous research, we focussed on facial and vocal attractiveness, which are known to be used in human mate choice and to carry concordant information regarding mate quality. Here we show that males with more attractive faces have more attractive voices as judged by female adults and adolescents, but not by female children. This suggests that cues of facial and vocal attractiveness provide similar information, but that awareness of these cues does not develop fully until reproductive capability, when mate choice judgments become relevant. Adolescents’ judgments also mirrored those of adults in that, like adults, they preferred lower‐pitched male voices, and as a group made concordant judgments about facial attractiveness. However, they did not make similarly concordant judgments about vocal attractiveness, suggesting that a further period of maturation and learning is required to fully develop optimal judgments for mate choice.     

Preferences for masculinity in male bodies change across the menstrual cycle

In human females cyclic shifts in preference have been documented for odour and physical and behavioral male traits. Women prefer the smell of dominant males, more masculine male faces and men behaving more dominantly when at peak fertility than at other times in their menstrual cycle. Here we examine variation in preferences for body sexual dimorphism. Across two studies, both between- and within-participant, we show that women prefer greater masculinity in male bodies at times when their fertility is likely highest, in the follicular phase of their cycle. Shifts were seen when rating for a short-term but not when rating for a long-term relationship. In line with studies showing similar effects for facial sexual dimorphism, we also show that women prefer greater masculinity when they think themselves attractive than when they think themselves less attractive. These results indicate that women's preferences for sexual dimorphism in male bodies follow a similar pattern as found for sexual dimorphism and dominance in other domains and such differences in preference may serve a similar function. Cyclic preferences could influence women to select partners when most likely to become pregnant that possess traits that may be most likely to maximize their offspring's quality via attraction to masculinity or serve to help acquire investment via attraction to femininity.     

Men's masculinity and attractiveness predict their female partners' reported orgasm frequency and timing

It has been hypothesized that female orgasm evolved to facilitate recruitment of high-quality genes for offspring. Supporting evidence indicates that female orgasm promotes conception, although this may be mediated by the timing of female orgasm in relation to male ejaculation. This hypothesis also predicts that women will achieve orgasm more frequently when copulating with high-quality males, but limited data exist to support this prediction. We therefore explored relationships between the timing and frequency of women's orgasms and putative markers of the genetic quality of their mates, including measures of attractiveness, facial symmetry, dominance, and masculinity. We found that women reported more frequent and earlier-timed orgasms when mated to masculine and dominant men—those with high scores on a principal component characterized by high objectively-measured facial masculinity, observer-rated facial masculinity, partner-rated masculinity, and partner-rated dominance. Women reported more frequent orgasm during or after male ejaculation when mated to attractive men—those with high scores on a principal component characterized by high observer-rated and self-rated attractiveness. Putative measures of men's genetic quality did not predict their mates' orgasms from self-masturbation or from non-coital partnered sexual behavior. Overall, these results appear to support a role for female orgasm in sire choice.     

Adiposity,compared with masculinity,serves as a more valid cue to immunocompetence in human mate choice

According to the ‘good genes’ hypothesis, females choose males based on traits that indicate the male''s genetic quality in terms of disease resistance. The ‘immunocompetence handicap hypothesis’ proposed that secondary sexual traits serve as indicators of male genetic quality, because they indicate that males can contend with the immunosuppressive effects of testosterone. Masculinity is commonly assumed to serve as such a secondary sexual trait. Yet, women do not consistently prefer masculine looking men, nor is masculinity consistently related to health across studies. Here, we show that adiposity, but not masculinity, significantly mediates the relationship between a direct measure of immune response (hepatitis B antibody response) and attractiveness for both body and facial measurements. In addition, we show that circulating testosterone is more closely associated with adiposity than masculinity. These findings indicate that adiposity, compared with masculinity, serves as a more important cue to immunocompetence in female mate choice.     

Sexual attractiveness shared by both sexes mediates same‐sex sexual behaviour in the parasitoid wasp Telenomus triptus

The mating behaviour of a quasi‐gregarious egg parasitoid Telenomus triptus Nixon (Hymenoptera: Platygastridae), which exploits egg masses of a stink bug Piezodorus hybneri (Heteroptera: Pentatomidae), is examined in the laboratory. In this parasitoid wasp, male adults that emerge earlier stay at the natal egg mass and mate with subsequently emerging females. In the present study, a male adult that encounters the emergence of another male always waits for it to egress, and then mounts the newly emerging male. To examine why males of T. triptus show same‐sex sexual behaviour, male adults are presented with a parasitized host egg mass or a freshly killed wasp. Male adults are observed to remain at host egg masses from which only male wasp(s) had emerged. In addition, male adults attempt to copulate with freshly killed young male wasps. It is suggested that newly emerging male wasps are targets of same‐sex sexual behaviour because they possess cues for male sexual behaviour similar to the cues of females. Both the sex and age of freshly killed wasps affect the frequency of the sexual behaviour of male adults: females are more attractive than males, although their attractiveness declines with age. When the mating opportunity is restricted to the natal egg mass, the costs of failing to notice newly emerging female adults should be extremely high. Therefore, males are forced not to discriminate the sex, resulting in same‐sex sexual behaviour.     

Evidence for the stress-linked immunocompetence handicap hypothesis in human male faces

The stress-linked immunocompetence handicap hypothesis (SL-ICHH) of sexual selection incorporates a role of the stress hormone corticosterone (C; cortisol in humans) in relationships between testosterone (T), immunity and secondary sexual trait expression. In support of this, C has been shown to mediate and moderate relationships between T and immune response and to be inversely related to attractiveness in some avian species. We predicted that female preferences for cues to T in human male faces would be contingent upon co-occurring cortisol levels. In study 1, we tested relationships between T and cortisol and attractiveness, masculinity and health ratings of raw male faces. We found cortisol to be inversely related to attractiveness. In study 2, we tested female preferences for male faces that were parametrically manipulated on the basis of cues to naturally co-occurring levels of T and cortisol across the menstrual cycle. Women preferred cues to low cortisol in general and in the fertile phase of the cycle, and there was an interaction between T and cortisol in general and in the non-fertile phase. Results were consistent with the SL-ICHH but not the original immunocompetence handicap model: females expressed preferences for cues to cortisol but not for cues to T, except in interaction with the stress hormone. Results inform the SL-ICHH by demonstrating female preferences for low cortisol and the nature of its interaction with T in humans, as well as indicating the traits that may be signalled by different combinations of the hormones including immune response, current health and resource acquisition characteristics.     

Manipulating Shape Cues in Dynamic Human Faces: Sexual Dimorphism is Preferred in Female but not Male Faces

Sexual dimorphism in the human face has been linked to attractiveness, and computer‐graphic techniques have been useful in this field by allowing experimental manipulation of dimorphism. However, a limitation of much research is its reliance on static pictorial stimuli, whereas real faces are dynamic, as is much courtship behaviour throughout nature. Furthermore, little is known about possible interactions between static and dynamic facial cues and attractiveness. We adapted well‐established face‐morphing technology to manipulate sexual dimorphism in male and female dynamic facial displays depicting prosocial and antisocial behaviour. Masculinised and feminised versions of these videos were presented as a two‐alternative forced choice task to measure preferences. Feminised female videos were preferred in both movement contexts, as expected. More surprisingly, no directional preference for masculinity or femininity was evident for the male videos in either context. Further analysis showed that the movement of the faces (prosocial vs. antisocial) had no effect on attractiveness ratings. Results were the same with static stimuli and did not conflict with findings from the wider literature using static faces. These findings suggest that the new technique we describe is a valid way to manipulate facial shape in videos and can now be widely applied to future studies of facial morphing.     

Colorful male guppies do not provide females with fecundity benefits

The phenotype-linked fertility hypothesis (PLFH) predicts thatmales with elaborated sexual ornaments signal their high fertilizingefficiency to females and that female preferences for ornamentedmales are driven by direct fecundity benefits. Although somestudies have demonstrated that attractive males produce moreor higher quality sperm, there is limited experimental evidencethat females derive fecundity benefits by mating with attractivemales. Some of the best indirect evidence for the PLFH comesfrom work on guppies (Poecilia reticulata), an internally fertilizingspecies of freshwater fish in which phenotypically attractivemales produce larger and relatively higher quality ejaculatesthan their less attractive counterparts. We used artificialinsemination to impregnate female guppies using known numbersof sperm from a range of males with different phenotypes andrelated female fecundity (brood success, time from inseminationto parturition, and brood size) to sperm numbers and male phenotype(body size and the relative area of color spots). We found noevidence that male phenotype or experimentally adjusted "ejaculate"size influenced any of our measures of female fecundity. Theseresults highlight the importance of experimentally investigatingpotential fecundity benefits associated with female mating preferencesbefore concluding that the maintenance of these preferencesis driven by the pursuit of such benefits.     

Low Pitched Voices Are Perceived as Masculine and Attractive but Do They Predict Semen Quality in Men?

Women find masculinity in men's faces, bodies, and voices attractive, and women's preferences for men's masculine features are thought to be biological adaptations for finding a high quality mate. Fertility is an important aspect of mate quality. Here we test the phenotype-linked fertility hypothesis, which proposes that male secondary sexual characters are positively related to semen quality, allowing females to obtain direct benefits from mate choice. Specifically, we examined women's preferences for men's voice pitch, and its relationship with men's semen quality. Consistent with previous voice research, women judged lower pitched voices as more masculine and more attractive. However men with lower pitched voices did not have better semen quality. On the contrary, men whose voices were rated as more attractive tended to have lower concentrations of sperm in their ejaculate. These data are more consistent with a trade off between sperm production and male investment in competing for and attracting females, than with the phenotype-linked fertility hypothesis.     

Effects of Age and Experience on Male Mate Choosiness

Mate choosiness by males has been documented in many taxa but we still do not know how it varies with age even though such variation can be important for our understanding of sexual selection on females. Theory provides conflicting predictions: young males, who are less attractive to females than older males, may be less choosy, or older males, who face fewer expected future mating opportunities, may be less choosy. In our experiments with fruit flies (Drosophila melanogaster), young (1‐d‐old) males spent relatively less time courting recently mated females than did mature (4‐d‐old) males. Overall, there was a gradual decline in male mate choosiness from age 1–7 d. As male age was correlated with the duration of deprivation from females, we tested for the effect of deprivation and found that same‐age males previously exposed to females were choosier than female‐deprived males. We also assessed key male parameters that could affect choosiness and found that, compared to mature males, young males were less attractive to females, less competitive in intramale interactions and less fertile. Although the lesser attractiveness and competitiveness should select for lesser mate choosiness in young males, their limited fertility and more expected future mating opportunities seem to override the other factors and lead to high mate choosiness in young males. Overall, our data indicate that young males just after reaching sexual maturity are choosy and that subsequent exposure to females can maintain high levels of male mate choosiness with age. Hence, males can contribute much more to sexual selection than previously appreciated.     

COSTLY SIGNALS IN A FIELD CRICKET CAN INDICATE HIGH‐ OR LOW‐QUALITY DIRECT BENEFITS DEPENDING UPON THE ENVIRONMENT

The handicap hypothesis proposes that male signals provide reliable information to females because only males of high condition provide high‐quality mating benefits and can afford the costs of producing attractive signals. In the context of direct benefits, the handicap hypothesis predicts that benefit quality and signal attractiveness will positively covary among genotypes, positively covary among environments, or be affected by congruent genotype–environment interactions. The latter should occur if the relative condition of a genotype is environment‐dependent. We tested these predictions in the variable field cricket, Gryllus lineaticeps. An interaction between male family and nutritional environment affected the expression of a costly signal preferred by females, while only male family affected direct benefit quality. These noncongruent effects of family and nutritional environment are inconsistent with the handicap hypothesis, and appear to have resulted from variation among nutritional environments in the relationship between signal attractiveness and benefit quality. Surprisingly, signal attractiveness was positively correlated with benefit quality when males experienced a low nutrition environment but negatively correlated with benefit quality when males experienced a high nutrition environment. As a result, female choice for direct benefits may be difficult, particularly in heterogeneous environments, unless females can assess the environmental histories of males.     

Reproductive strategy, sexual development and attraction to facial characteristics

Sexual reproduction strategies vary both between and within species in the level of investment in offspring. Life-history theories suggest that the rate of sexual maturation is critically linked to reproductive strategy, with high investment being associated with few offspring and delayed maturation. For humans, age of puberty and age of first sex are two developmental milestones that have been associated with reproductive strategies. Stress during early development can retard or accelerate sexual maturation and reproduction. Early age of menarche is associated with absence of younger siblings, absence of a father figure during early life and increased weight. Father absence during early life is also associated with early marriage, pregnancy and divorce. Choice of partner characteristics is critical to successful implementation of sexual strategies. It has been suggested that sexually dimorphic traits (including those evident in the face) signal high-quality immune function and reproductive status. Masculinity in males has also been associated with low investment in mate and offspring. Thus, women's reproductive strategy should be matched to the probability of male investment, hence to male masculinity. Our review leads us to predict associations between the rate of sexual maturation and adult preferences for facial characteristics (enhanced sexual dimorphism and attractiveness). We find for men, engaging in sex at an early age is related to an increased preference for feminized female faces. Similarly, for women, the earlier the age of first sex the greater the preference for masculinity in opposite-sex faces. When we controlled sexual dimorphism in male faces, the speed of sexual development in women was not associated with differences in preference for male facial attractiveness. These developmental influences on partner choice were not mediated by self-rated attractiveness or parental relationships. We conclude that individuals assort in preferences based on the rapidity of their sexual development. Fast developing individuals prefer opposite-sex partners with an increased level of sexually dimorphic facial characteristics.     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.