Genetic diversity revealed in human faces

From an evolutionary perspective, human facial attractiveness is proposed to signal mate quality. Using a novel approach to the study of the genetic basis of human preferences for facial features, we investigated whether attractiveness signals mate quality in terms of genetic diversity. Genetic diversity in general has been linked to fitness and reproductive success, and genetic diversity within the major histocompatibility complex (MHC) has been linked to immunocompetence and mate preferences. We asked whether any preference for genetic diversity is specific to MHC diversity or reflects a more general preference for overall genetic diversity. We photographed and genotyped 160 participants using microsatellite markers situated within and outside the MHC, and calculated two measures of genetic diversity: mean heterozygosity and standardized mean d(2). Our results suggest a special role for the MHC in female preferences for male faces. MHC heterozygosity positively predicted male attractiveness, and specifically facial averageness, with averageness mediating the MHC-attractiveness relationship. For females, standardized mean d(2) at non-MHC loci predicted facial symmetry. Thus, attractive facial characteristics appear to provide visual cues to genetic quality in both males and females, supporting the view that face preferences have been shaped by selection pressures to identify high-quality mates.     

Male Sailfin mollies (Poecilia latipinna) copy the mate choice of other males

Female mate-copying has been shown to occur between heterospecifics:female sailfin mollies Poecilia latipinna copy the choice oftheir gynogenetic associates, Amazon mollies P. formosa. Femalemate-copying thus contributes to the maintenance of this asexual-sexualspecies complex by providing an advantage to male sailfin molliesthat mate with Amazon females; because of mate-copying thesemales increase their attractiveness to conspecific females.Here we show that male mate-copying, an unreported phenomenon,also occurs and that it can reverse male preferences for conspecificfemales. Male mate-copying should also contribute to the maintenanceof gynogens and might be advantageous in allowing males a meansto rapidly assess female receptivity although sometimes resultingin heterospedfic matings.     

Female mate preferences on high‐dimensional shape variation for male species recognition traits

Females in many animal species must discriminate between conspecific and heterospecific males when choosing mates. Such mating preferences that discriminate against heterospecifics may inadvertently also affect the mating success of conspecific males, particularly those with more extreme phenotypes. From this expectation, we hypothesized that female mate choice should cause Enallagma females (Odonata: Coenagrionidae) to discriminate against conspecific males with more extreme phenotypes of the claspers males use to grasp females while mating – the main feature of species mate recognition in these species. To test this, we compared cerci sizes and shapes between males that were captured while mating with females to males that were captured at the same time but not mating in three Enallagma species. In contrast to our hypothesis, we found only one of forty comparisons of shape variation that was consistent with females discriminating against males with more extreme cerci shapes. Instead, differences in cerci shape between mating and single males suggested that females displayed directional preferences on 1–4 aspects of cerci shape in two of the species in our samples. These results suggest that whereas some directional biases in mating based on cerci shape occur, the intraspecific phenotypic variation in male cerci size and shape is likely not large enough for females to express any significant incidental discrimination among conspecifics with more extreme shapes.     

Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes

Speciation by sexual selection is generally modeled as the coevolution of female preferences and elaborate male ornaments leading to behavioral (sexual) reproductive isolation. One prediction of these models is that female preference for conspecific males should evolve earlier than male preference for conspecific females in sexually dimorphic species with male ornaments. We tested that prediction in darters, a diverse group of freshwater fishes with sexually dimorphic ornamentation. Focusing on the earliest stages of divergence, we tested preference for conspecific mates in males and females of seven closely related species pairs. Contrary to expectation, male preference for conspecific females was significantly greater than female preference for conspecific males. Males in four of the 14 species significantly preferred conspecific females; whereas, females in no species significantly preferred conspecific males. Relationships between the strength of preference for conspecifics and genetic distance revealed no difference in slope between males and females, but a significant difference in intercept, also suggesting that male preference evolves earlier than females’. Our results are consistent with other recent studies in darters and suggest that the coevolution of female preferences and male ornaments may not best explain the earliest stages of behavioral isolation in this lineage.     

Prey Habitat Location by the Cassava Mealybug Predator Exochomus flaviventris: Olfactory Responses to Odor of Plant, Mealybug, Plant–Mealybug Complex, and Plant–Mealybug–Natural Enemy Complex

Exochomus flaviventris Mader is considered to be the most active predator of the cassava mealybug Phenacoccus manihoti Matile–Ferrero in Central Africa. The response of experienced gravid female coccinellids to the odor of cassava plant (var. Zanaga), unparasitized mealybugs, plant–mealybug complex with or without feeding prey (parasitized or not), and plant–mealybug complex with or without conspecific coccinellids was investigated in a Y-tube olfactometer. The odor of uninfested cassava plants was not more attractive than clean air. Dual-choice tests revealed that mealybug-infested plants were preferred to mealybugs alone and mealybug-damaged plants and were the major sources of volatiles that attract females coccinellids to the microhabitat of its prey. The emission of volatile chemicals did not appear to be limited to the infested parts of the plant but did occur systemically throughout the plant. The presence of conspecific coccinellid larvae or adult males did not modify the attractiveness of the mealybug-infested plants. However, when an infested plant with conspecific predator females (alone or with conspecific males) was compared to an infested plant or infested plant with conspecific males, E. flaviventris females showed a preference for the last two sources of odor. The uninfested plant with conspecific males was also preferred to the uninfested plant with conspecific females. In addition, the odor of conspecific males was preferred over that of conspecific females. Female predators preferred the plant infested with unparasitized mealybugs over the plant infested with mealybugs previously parasitized. These results showed that E. flaviventris females use herbivore-induced plant volatiles during foraging and can detect via olfaction the presence of conspecific gravid females and parasitized prey, thus assessing patch suitability from a distance.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

The presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.     

Visible skin color distribution plays a role in the perception of age, attractiveness, and health in female faces

Evolutionary psychologists have proposed that preferences for facial characteristics, such as symmetry, averageness, and sexual dimorphism, may reflect adaptations for mate choice because they signal aspects of mate quality. Here, we show that facial skin color distribution significantly influences the perception of age and attractiveness of female faces, independent of facial form and skin surface topography. A set of three-dimensional shape-standardized stimulus faces—varying only in terms of skin color distribution due to variation in biological age and cumulative photodamage—was rated by a panel of naive judges for a variety of perceptual endpoints relating to age, health, and beauty. Shape- and topography-standardized stimulus faces with the homogeneous skin color distribution of young people were perceived as younger and received significantly higher ratings for attractiveness and health than analogous stimuli with the relatively inhomogeneous skin color distribution of more elderly people. Thus, skin color distribution, independent of facial form and skin surface topography, seems to have a major influence on the perception of female facial age and judgments of attractiveness and health as they may signal aspects of underlying physiological condition of an individual relevant for mate choice. We suggest that studies on human physical attractiveness and its perception need to consider the influence of visible skin condition driven by color distribution and differentiate between such effects and beauty-related traits due to facial shape and skin topography.     

Symmetry and Human Facial Attractiveness

Symmetry may act as a marker of phenotypic and genetic quality and is preferred during mate selection in a variety of species. Measures of human body symmetry correlate with attractiveness, but studies manipulating human face images report a preference for asymmetry. These results may reflect unnatural feature shapes and changes in skin textures introduced by image processing. When the shape of facial features is varied (with skin textures held constant), increasing symmetry of face shape increases ratings of attractiveness for both male and female faces. These findings imply facial symmetry may have a positive impact on mate selection in humans.     

Bearded reedlings adjust their pair-bond behaviour in relation to the sex and attractiveness of unpaired conspecifics

An individual's investment in mating or keeping a pair bond intact may be influenced not only by the attractiveness of its current mate, but also by that of other potential mates. In this study, we investigated the effect of relative attractiveness on pair-bond behaviour in bearded reedlings, Panurus biarmicus. We showed that mate attractiveness, in terms of beard length in males and tail length in females, influenced courtship behaviour when the pair was kept isolated. In the presence of a conspecific, contact initiations within a pair increased. This increment was mainly related to the sex of the unpaired conspecific, however, and less to differences in attractiveness between the current partner and the unpaired conspecific. Female contact initiations towards potential extra mates were independent of male attractiveness, whereas male contact behaviour was significantly influenced by female attractiveness. However, females displayed more contact initiations to their current mate when they were less attractive than the unpaired females. Males decreased their overtures towards other females with increasing attractiveness of their current mates. Overall, our results suggested that, when there was a risk of losing their mate, bearded reedlings adjust their pair-bond investment mainly in response to the presence or absence of a competitor, and fine-tune investment to a lesser extent in response to the attractiveness of that potential competitor.     

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.     

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.     

Developmental changes in children's facial preferences

Facial averageness, symmetry, health, and femininity are positively associated with adults' judgements of attractiveness, but little is known about the age at which preferences for individual facial traits develop. We investigated preferences for these facial traits and global attractiveness in 4- to 17-year-olds (N = 346). All age groups showed preferences for globally attractive faces. Preferences for averageness, symmetry, and health did not emerge until middle childhood and experienced apparent disruption or stasis around age 10- to 14-years; femininity was not preferred until early adulthood, and this preference was seen only in girls. Children's pubertal development was not clearly related to any facial preferences, but the results are consistent with the suggestion that early adrenal hormone release may play an activating role in mate preferences, while other constraints may delay further increases in preferences during later puberty.     

Human body odour, symmetry and attractiveness.

Several studies have found body and facial symmetry as well as attractiveness to be human mate choice criteria. These characteristics are presumed to signal developmental stability. Human body odour has been shown to influence female mate choice depending on the immune system, but the question of whether smell could signal general mate quality, as do other cues, was not addressed in previous studies. We compared ratings of body odour, attractiveness, and measurements of facial and body asymmetry of 16 male and 19 female subjects. Subjects wore a T-shirt for three consecutive nights under controlled conditions. Opposite-sex raters judged the odour of the T-shirts and another group evaluated portraits of the subjects for attractiveness. We measured seven bilateral traits of the subject's body to assess body asymmetry. Facial asymmetry was examined by distance measurements of portrait photographs. The results showed a significant positive correlation between facial attractiveness and sexiness of body odour for female subjects. We found positive relationships between body odour and attractiveness and negative ones between smell and body asymmetry for males only if female odour raters were in the most fertile phase of their menstrual cycle. The outcomes are discussed in the light of different male and female reproductive strategies.     

Size-dependent response to conspecific mating calls by male crickets.

Male sexual displays provide females with information that is crucial to their reproductive decisions. That same information is available to eavesdroppers, with potential consequences for both signaller and receiver. We present empirical evidence for size-dependent responses to intersexual communication by conspecific rivals. Acoustic features of a male house cricket's (Acheta domesticus) mating call are positively associated with its size, with females preferring the calls of larger males. In order to investigate whether conspecific males make use of the information content of mating calls, we examined their phonotactic responses to call recordings that differ in attractiveness to females. Males of all sizes exhibited positive phonotaxis, with smaller males showing a clear preference for female-preferred calls. Smaller males were also less likely to seek contact with the speaker playing their chosen call. We discuss possible explanations for this size-dependent male behaviour.     

Facial attractiveness, symmetry and cues of good genes.

Cues of phenotypic condition should be among those used by women in their choice of mates. One marker of better phenotypic condition is thought to be symmetrical bilateral body and facial features. However, it is not clear whether women use symmetry as the primary cue in assessing the phenotypic quality of potential mates or whether symmetry is correlated with other facial markers affecting physical attractiveness. Using photographs of men's faces, for which facial symmetry had been measured, we found a relationship between women's attractiveness ratings of these faces and symmetry, but the subjects could not rate facial symmetry accurately. Moreover, the relationship between facial attractiveness and symmetry was still observed, even when symmetry cues were removed by presenting only the left or right half of faces. These results suggest that attractive features other than symmetry can be used to assess phenotypic condition. We identified one such cue, facial masculinity (cheek-bone prominence and a relatively longer lower face), which was related to both symmetry and full- and half-face attractiveness.     

Viewing time as a measure of sexual interest

Based on the hypothesis that unobtrusively measured viewing time reflects sexual interest, it was predicted that viewing times should correlate with ratings of sexual attractiveness and with phallometrically measured age and gender preferences. Four additional predictions were derived from the Symons (1979) evolutionary theory of human mate preferences: (1) male and female subjects should view slides of young adults of the opposite sex longest and adults of the same sex and prepubescent children of both sexes the shortest, (2) the correlation between viewing time and sexual attractiveness ratings should be higher among males than females (3) males should look at slides of pubescent females longer than females look at slides of pubescent males, and (4) males should look longer at adult females than females look at adult males. Two studies involving 24 heterosexual females and 58 heterosexual males provided statistically significant support for all predictions except the last one.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

Cross-Cultural Agreement in Facial Attractiveness Preferences: The Role of Ethnicity and Gender

Previous work showed high agreement in facial attractiveness preferences within and across cultures. The aims of the current study were twofold. First, we tested cross-cultural agreement in the attractiveness judgements of White Scottish and Black South African students for own- and other-ethnicity faces. Results showed significant agreement between White Scottish and Black South African observers'' attractiveness judgements, providing further evidence of strong cross-cultural agreement in facial attractiveness preferences. Second, we tested whether cross-cultural agreement is influenced by the ethnicity and/or the gender of the target group. White Scottish and Black South African observers showed significantly higher agreement for Scottish than for African faces, presumably because both groups are familiar with White European facial features, but the Scottish group are less familiar with Black African facial features. Further work investigating this discordance in cross-cultural attractiveness preferences for African faces show that Black South African observers rely more heavily on colour cues when judging African female faces for attractiveness, while White Scottish observers rely more heavily on shape cues. Results also show higher cross-cultural agreement for female, compared to male faces, albeit not significantly higher. The findings shed new light on the factors that influence cross-cultural agreement in attractiveness preferences.     

Male facial attractiveness and masculinity may provide sex‐ and culture‐independent cues to semen quality

Phenotype‐linked fertility hypothesis (PLFH) predicts that male secondary sexual traits reveal honest information about male fertilization ability. However, PLFH has rarely been studied in humans. The aim of the present study was to test PLFH in humans and to investigate whether potential ability to select fertile partners is independent of sex or cultural background. We found that on the contrary to the hypothesis, facial masculinity was negatively associated with semen quality. As increased levels of testosterone have been demonstrated to impair sperm production, this finding may indicate a trade‐off between investments in secondary sexual signalling (i.e. facial masculinity) and fertility or status‐dependent differences in investments in semen quality. In both sexes and nationalities (Spanish and Colombian), ranked male facial attractiveness predicted male semen quality. However, Spanish males and females estimated facial images generally more attractive (gave higher ranks) than Colombian raters, and in both nationalities, males gave higher ranks than females. This suggests that male facial cues may provide culture‐ and sex‐independent information about male fertility. However, our results also indicate that humans may be more sensitive to facial attractiveness cues within their own populations and also that males may generally overestimate the attractiveness of other men to females.