Copulatory and Postcopulatory Sexual Selection in Primates.

Many aspects of primate reproductive anatomy and physiology have been influenced by copulatory and postcopulatory sexual selection, especially so in taxa where multiple-partner matings by females result in the sperm of rival males competing for access to a given set of ova (sperm competition). However, the female reproductive system also exerts profound effects upon sperm survival, storage and transport, raising the possibility that female traits influence male reproductive success (via cryptic female choice). Current knowledge of sperm competition and cryptic choice in primates and other mammals is reviewed here. The relevance of these comparative studies to our understanding of human reproduction and evolution is discussed.

Male-Male Mounting Behaviour in Free-Ranging Golden Snub-Nosed Monkeys (Rhinopithecus roxellana).

An all-male band of golden snub-nosed monkeys (Rhinopithecus roxellana) was observed for 3 months in the Qinling Mountains of China, in order to collect data on the frequencies and contextual significance of male-male mounting behaviour. Mounts occurred in a variety of affiliative, dominance-related and sexual contexts, which differed depending upon the ages of the males involved. Mounting behaviour in this group was mainly initiated by adults. Juveniles mounted each other in affiliative contexts (during play and prior to grooming). Adult males mounted subadult and juvenile partners in a greater variety of sociosexual contexts (dominance/rank-related interactions; reconciliation following agonistic encounters, and sometimes as a prelude to receiving grooming). However, subadults and juveniles were never observed to mount adults. In one dyad, involving an adult male and a subadult partner, mounting was more frequent and prolonged, and included bouts of deep pelvic thrusting. Two mounts resulted in anal intromissions and, in 1 case, the subadult partner exhibited seminal emission. Given that the study took place during the annual mating peak period of R. roxellana, it is possible that this unusual male-male sexual activity was related to the absence of mating opportunities for those adults that were excluded from 1-male units.

The Role of Breast Size and Areolar Pigmentation in Perceptions of Women's Sexual Attractiveness, Reproductive Health, Sexual Maturity, Maternal Nurturing Abilities, and Age.

Women's breast morphology is thought to have evolved via sexual selection as a signal of maturity, health, and fecundity. While research demonstrates that breast morphology is important in men's judgments of women's attractiveness, it remains to be determined how perceptions might differ when considering a larger suite of mate relevant attributes. Here, we tested how variation in breast size and areolar pigmentation affected perceptions of women's sexual attractiveness, reproductive health, sexual maturity, maternal nurturing abilities, and age. Participants (100 men; 100 women) rated images of female torsos modeled to vary in breast size (very small, small, medium, and large) and areolar pigmentation (light, medium, and dark) for each of the five attributes listed above. Sexual attractiveness ratings increased linearly with breast size, but large breasts were not judged to be significantly more attractive than medium-sized breasts. Small and medium-sized breasts were rated as most attractive if they included light or medium colored areolae, whereas large breasts were more attractive if they had medium or dark areolae. Ratings for perceived age, sexual maturity, and nurturing ability also increased with breast size. Darkening the areolae reduced ratings of the reproductive health of medium and small breasts, whereas it increased ratings for large breasts. There were no significant sex differences in ratings of any of the perceptual measures. These results demonstrate that breast size and areolar pigmentation interact to determine ratings for a suite of sociosexual attributes, each of which may be relevant to mate choice in men and intra-sexual competition in women.

Eye tracking of men's preferences for female breast size and areola pigmentation.

Sexual selection via male mate choice has often been implicated in the evolution of permanently enlarged breasts in women. While questionnaire studies have shown that men find female breasts visually attractive, there is very little information about how they make such visual judgments. In this study, we used eye-tracking technology to test two hypotheses: (1) that larger breasts should receive the greatest number of visual fixations and longest dwell times, as well as being rated as most attractive; (2) that lightly pigmented areolae, indicative of youth and nubility, should receive most visual attention and be rated as most attractive. Results showed that men rated images with medium-sized or large breasts as significantly more attractive than small breasts. Images with dark and medium areolar pigmentation were rated as more attractive than images with light areolae. However, variations in breast size had no significant effect on eye-tracking measures (initial visual fixations, number of fixations, and dwell times). The majority of initial fixations during eye-tracking tests were on the areolae. However, areolar pigmentation did not affect measures of visual attention. While these results demonstrate that cues indicative of female sexual maturity (large breasts and dark areolae) are more attractive to men, patterns of eye movements did not differ based on breast size or areolar pigmentation. We conclude that areolar pigmentation, as well as breast size, plays a significant role in men's judgments of female attractiveness. However, fine-grained measures of men's visual attention to these morphological traits do not correlate, in a simplistic way, with their attractiveness judgments.

Eye-tracking of men's preferences for waist-to-hip ratio and breast size of women.

Studies of human physical traits and mate preferences often use questionnaires asking participants to rate the attractiveness of images. Female waist-to-hip ratio (WHR), breast size, and facial appearance have all been implicated in assessments by men of female attractiveness. However, very little is known about how men make fine-grained visual assessments of such images. We used eye-tracking techniques to measure the numbers of visual fixations, dwell times, and initial fixations made by men who viewed front-posed photographs of the same woman, computer-morphed so as to differ in her WHR (0.7 or 0.9) and breast size (small, medium, or large). Men also rated these images for attractiveness. Results showed that the initial visual fixation (occurring within 200 ms from the start of each 5 s test) involved either the breasts or the waist. Both these body areas received more first fixations than the face or the lower body (pubic area and legs). Men looked more often and for longer at the breasts, irrespective of the WHR of the images. However, men rated images with an hourglass shape and a slim waist (0.7 WHR) as most attractive, irrespective of breast size. These results provide quantitative data on eye movements that occur during male judgments of the attractiveness of female images, and indicate that assessments of the female hourglass figure probably occur very rapidly.

Men's preferences for women's breast morphology in New Zealand, Samoa, and Papua New Guinea.

Sexual selection via mate choice may have influenced the evolution of women's breast morphology. We conducted an image-based questionnaire quantifying and comparing the preferences of men from Papua New Guinea (PNG), Samoa, and New Zealand (NZ) for images of women's breast size, breast symmetry, areola size, and areolar pigmentation. Results showed that men from PNG preferred larger breasts to a greater extent than men from Samoa and NZ, providing some support for the hypothesis that men from subsistence living cultures have a greater preference for morphological cues indicative of caloric reserves. Symmetrical breasts were most attractive to men in each culture. However, preferences were highest among NZ men, followed by men from Samoa, and were lowest among men from PNG. These results did not support the hypothesis that people living in higher pathogen environments have a greater preference for traits indicative of pathogen resistance and developmental stability. Large areolae were preferred among men from PNG, and to a lesser extent in Samoa, while in NZ men preferred medium-sized areolae. Thus, men's preferences for women's areolar size appear to be highly culturally specific. Darkly pigmented areolae were most attractive to men from Samoa and PNG, whereas men from NZ preferred areolae with medium pigmentation. These findings suggest that areolar pigmentation indicative of sexual maturity is preferred by men rather than lighter pigmentation, which may signal that a woman is in the early years of reproductive maturity. This study highlights the importance of cross-cultural research when testing the role of morphological cues in mate choice.

Human physique and sexual attractiveness in men and women: a New Zealand-U.S. comparative study.

Men and women living in New Zealand and California completed five studies regarding human physique and sexual attractiveness. In Studies 1-3, women rated images of male stimuli and, in Studies 4-5, men rated female stimuli. In Study 1, women in both countries rated mesomorphic (muscular) and average male somatotypes as most attractive, followed by ectomorphic (slim) and endomorphic (heavily built) figures. In Study 2, amount and distribution of masculine trunk hair (chest and abdominal) was altered progressively in a series of front-posed male figures. In both countries, the image lacking any trunk hair was rated as the most attractive, with a steady decline in attractiveness as hirsutism became more pronounced. Study 3 assessed attractiveness of front-posed male figures that varied only in the length of the non-erect penis. Five lengths were presented: The smallest penile size was rated as less attractive than three intermediate sizes. The largest penile size was not the most attractive, but received higher scores than the unaltered and smallest penile size. In Study 4, men rated the attractiveness of back-posed female images varying in waist-to-hip ratio (WHR) (from 0.5 to 1.0). The 0.7 WHR figure was rated more attractive in New Zealand and the 0.6 WHR in California. Study 5 measured the attractiveness of female skin color; men expressed preferences for lighter skinned female figures in New Zealand and California. Results indicate very similar preferences for sexually dimorphic physical traits among men and women of European extraction, living in two culturally and geographically different environments.

Male preferences for female waist-to-hip ratio and body mass index in the highlands of Papua New Guinea.

One hundred men, living in three villages in a remote region of the Eastern Highlands of Papua New Guinea were asked to judge the attractiveness of photographs of women who had undergone micrograft surgery to reduce their waist-to-hip ratios (WHRs). Micrograft surgery involves harvesting adipose tissue from the waist and reshaping the buttocks to produce a low WHR and an "hourglass" female figure. Men consistently chose postoperative photographs as being more attractive than preoperative photographs of the same women. Some women gained, and some lost weight, postoperatively, with resultant changes in body mass index (BMI). However, changes in BMI were not related to men's judgments of attractiveness. These results show that the hourglass female figure is rated as attractive by men living in a remote, indigenous community, and that when controlling for BMI, WHR plays a crucial role in their attractiveness judgments.

Sexual behavior, reproductive physiology and sperm competition in male mammals.

Sperm competition involves competition between the gametes of two or more males of a species for fertilization of a given set of ova. Sperm competition is widespread among mammals, as in many other groups of vertebrates. Effects of sexual selection, via sperm competition, upon the evolution of reproductive physiology and behavior are much better understood in invertebrates (and especially in insects) than is the case for mammals. However, if the reproductive organs of male mammals are viewed as an integrated system for production and delivery of spermatozoa (and accessory glandular secretions) to females, then it is logical to assume that sperm competition might influence the evolution of all parts of the system, as well as associated physiological mechanisms (e.g., testicular endocrinology) and behavior (e.g., copulatory patterns). Here we analyze and review relationships between mating systems, relative testes sizes and sperm morphology, phallic morphology, circulating testosterone levels and sexual behavior in male mammals.

Studies of human physique and sexual attractiveness: sexual preferences of men and women in China.

Men and women at Northwest University (n = 631), Xi'an, China, were asked to rate the attractiveness of male or female figures manipulated to vary somatotype, waist-to-hip ratio (WHR), secondary sexual traits, and other features. In study 1, women rated the average masculine somatotype as most attractive, followed by the mesomorphic (muscular), ectomorphic (slim), and endomorphic (heavily built) somatotypes, in descending order of preference. In study 2, the amount and distribution of masculine trunk (chest and abdominal) hair were altered progressively in a series of front-posed figures. Women rated figures with no or little trunk hair as most attractive. Study 3 assessed the attractiveness of front-posed male figures which varied only in length of their nonerect penis. Numerical ratings for this trait were low, but moderate lengthening of the penis (22% or 33% above average) resulted in a significant increase in scores for attractiveness. In study 4, Chinese men rated the attractiveness of back-posed female images varying in waist-to-hip ratio (WHR from 0.5-1.0). The 0.6 WHR figure was most preferred, followed by 0.7, while figures with higher ratios (0.9 or 1.0) were significantly less attractive. Study 5 rated the attractiveness of female skin color: men expressed a marked preference for images which were lighter in color, as compared to images of average or darker skin colors. These results, the first of their kind reported for a Chinese population, support the view that sexual selection has influenced the evolution of human physique and sexual attractiveness in men and women.

Human physique and sexual attractiveness: sexual preferences of men and women in Bakossiland, Cameroon.

Men and women living in a rural community in Bakossiland, Cameroon were asked to rate the attractiveness of images of male or female figures manipulated to vary in somatotype, waist-to-hip ratio (WHR), secondary sexual traits, and other features. In Study 1, women rated mesomorphic (muscular) and average male somatotypes as most attractive, followed by ectomorphic (slim) and endomorphic (heavily built) figures. In Study 2, amount and distribution of masculine trunk (chest and abdominal) hair was altered progressively in a series of front-posed male figures. A significant preference for one of these images was found, but the most hirsute figure was not judged as most attractive. Study 3 assessed attractiveness of front-posed male figures which varied only in length of the non-erect penis. Extremes of penile size (smallest and largest of five images) were rated as significantly less attractive than three intermediate sizes. In Study 4, Bakossi men rated the attractiveness of back-posed female images varying in WHR (from 0.5-1.0). The 0.8 WHR figure was rated markedly more attractive than others. Study 5 rated the attractiveness of female skin color. Men expressed no consistent preference for either lighter or darker female figures. These results are the first of their kind reported for a Central African community and provide a useful cross-cultural perspective to published accounts on sexual selection, human morphology and attractiveness in the U.S., Europe, and elsewhere.

Functional evidence for differences in sperm competition in humans and chimpanzees.

Sperm competition occurs when the gametes of or more males compete for opportunities to fertilize a given set of ova. Previous studies have demonstrated that certain morphological characteristics are affected by sperm competition intensity (e.g. relative testes size and sperm midpiece volume). This study examined whether aspects of sperm energetics may also be affected by sexual selection. We compared the membrane potential of mitochondria in live sperm between H. sapiens (single partner mating system) and P. troglodytes (multiple partner mating system). Flow cytometry of sperm stained with the carbocyanine fluorescent dye JC-1 (an assay for mitochondrial membrane potential) revealed marked differences in red fluorescence intensity. P. troglodytes sperm showed significantly higher mitochondrial membrane potential. Mitochondria provide a substantial part of the energy required for sperm motility. A higher mitochondrial loading may therefore be associated with enhanced sperm motility and/or longevity. Additionally, examination of JC-1 red fluorescence levels before and after in vitro capacitation revealed further differences. Whereas chimpanzee sperm showed maintenance of membrane potential after capacitation (in some cases even an increase), sperm from humans consistently showed reduction in membrane potential. These results indicate that the sperm of human beings and chimpanzees exhibit marked differences in mitochondrial function, which are affected by selection pressures relating to sperm competition and that these pressures differ significantly between humans and chimpanzees.

Social organization of the Milne-Edward's potto.

Nocturnal prosimian primates are often seen alone during their nocturnal activities, and are therefore categorized as "solitary". Recent research has shown that these animals actually possess social networks that differ among species. Here we present new information on one of the lesser studied prosimian primates, the potto, derived from fieldwork in Cameroon that employed radiotelemetry and behavioral observations. An analysis of association patterns and home-range overlaps between animals revealed that pottos associated more frequently with conspecifics than expected for a supposedly solitary primate. Certain males and females that were seen together regularly throughout the study, but were not observed to have contact with other pottos of the opposite sex, were labeled as "pairs". These pairs were found to have higher levels of association with each other than with other conspecifics. The only affiliative and sexual behaviors observed between members of the opposite sex occurred within the pairs of pottos. Although given the secretive nature of these primates, the possibility of extrapair copulations cannot be ruled out, their relatively small testis size indicates that sperm competition is not so important for this species.

The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta).

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.

Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx).

Previous research on semifree-ranging mandrills has shown that the degree of secondary sexual development differs among adult males. While some males are social, brightly colored, and have large testes and high levels of plasma testosterone, other males are peripheral or solitary, and lack fully developed secondary sexual features. In order to determine how these differences among males arise, and to investigate the influence of social factors, we examined the adolescent development of 13 semifree-ranging male mandrills of known age. Testicular volume began to increase markedly at 5.5 yr, and males began to develop secondary sexual adornments at the age of 6 yr. Males attained adult size and secondary sexual development at an average age of 9 yr. As males developed, they peripheralized, decreasing from 100% group-associated at 5 yr to 20% at 8 yr. At 9 yr some males reentered the social group and attained alpha rank, while others remained peripheral or solitary. Within this average development, there was marked variation among males in the timing of development. Adolescent males that were dominant for their age had higher testosterone levels, larger testes, and more advanced secondary sexual development than subordinate males. The implications of these findings are discussed in the light of differences that occur among adult males, male-male competition, and the evolution of secondary sexual adornments in this species.

Sperm competition: motility and the midpiece in primates.

In animals with multiple-partner mating systems, the gametes of two or more males must compete to fertilize a given set of ova. Here we show that the volume of the midpiece in individual sperm is significantly greater in primate species in which the females mate with multiple partners, and in which males have larger testes in relation to their body weight, than in those species that mate with only one partner and have relatively small testes. Our results indicate that sexual selection by sperm competition has influenced the evolution of a specific component of male-gamete morphology, the volume of the sperm midpiece.

Observations on genital morphology and anatomy of a hybrid male muriqui (genus Brachyteles).

The reproductive anatomy of the muriqui (genus Brachyteles) is poorly known. This paper describes the anatomy of the testis, penis and striated penile muscles in a young adult (5.25-year-old) captive-born muriqui which died at the Rio Primate Center. Two forms of muriqui occur in the Atlantic coastal forests of Brazil, and both are endangered. The form which is found north of 21 degrees 00' S latitude is classified as B. hypoxanthus by some authorities and is considered to be a species separate from B. arachnoides. The male specimen described here was a hybrid (the sire was B. arachnoides and the mother B. hypoxanthus). Hybridization was associated with absence of spermatozoa in the testis and with degeneration of the seminiferous epithelium. The structure of the prominent penis and striated penile muscles is discussed in relation to patterns of copulatory behavior and the likely occurrence of sperm competition in the muriqui. In addition, the occurrence of a baculum (os penis) is confirmed for this genus, and the first description of its morphology is provided.

Masculine somatotype and hirsuteness as determinants of sexual attractiveness to women.

Five questionnaire studies asked women to rate the attractiveness of outline drawings of male figures that varied in somatotype, body proportions, symmetry, and in distribution of trunk hair. In Study 1, back-posed figures of mesomorphic (muscular) somatotypes were rated as most attractive, followed by average, ectomorphic (slim), and endomorphic (heavily built) figures by both British and Sri Lankan women. In Study 2, computer morphing of somatotypes to produce an intergraded series resulted in a graded response in terms of perceived attractiveness which mirrored the findings of Study 1. In Study 3, back-posed figures were manipulated in order to change waist-to-hip ratios (WHR) and waist-to-shoulder ratios (WSR). A WHR of 0.8-0.9 and a WSR of 0.6 were rated as most attractive and these effects were more pronounced when modeling mesomorphic figures. In Study 4, symmetric figures of a mesomorphic somatotype were rated as less attractive than a normal (asymmetric) version of the same man. Study 5 showed that presence of trunk hair had a marked, positive effect upon women's ratings of attractiveness for both mesomorphic and endomorphic male figures. Women also judged figures with trunk hair as being older and they consistently rated endomorphic figures as being older than mesomorphs. These results are consistent with effects of sexual selection upon visual signals that advertise health, physical prowess, age, and underlying endocrine condition in the human male.