Primate mating systems and the evolution of immune response.

White blood cell (WBC) and red blood cell (RBC) counts were examined in a sample comprising 762 specimens, representing 25 genera and 38 species of captive non-human primates. Animals suffering from illnesses exhibited higher WBC counts than healthy specimens sampled during routine health checks. Analysis of basal WBC counts in healthy animals confirmed a positive correlation between higher cell counts and occurrences of multiple partner mating. This finding remained statistically significant after use of comparative analysis of independent contrasts (CAIC) to control for possible phylogenetic biases in the dataset. These findings were confirmed when using relative testis size as an independent index of mating system. By contrast, RBC counts were not significantly affected by health or correlated with mating systems. These studies confirm a correlation between WBC counts and primate mating systems, and extend the findings to include a positive correlation between WBC counts and relative testis size. However, the findings do not prove that a causal relationship between these variables exists. Further research is required to establish the evolutionary causation of basal WBC counts in primates.

Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx).

We present body mass (N = 419) and crown-rump length (CRL, N = 210) measurements from 38 male and 49 female mandrills born into a semifree-ranging colony in order to describe growth from birth to adulthood, and to investigate maternal influences upon growth. Adult male mandrills are 3.4 times the body mass, and 1.3 times the CRL, of adult females. Body mass dimorphism arises from a combination of sex differences in length of the growth period (females attain adult body mass at 7 years, males at 10 years) and growth rate. Both sexes undergo a subadult growth spurt in body mass, and this is much more dramatic in males (peak velocity 551 g/months +/- 89 SEM at 84-96 months). CRL dimorphism arises from bimaturism (females attain adult CRL at 6 years, males after 10 years), and neither sex shows a particular subadult growth spurt in CRL. Sexual size dimorphism thus represents important time and metabolic costs to males, who mature physically approximately 3-4 years after females. Considerable interindividual variation occurs in the size-for-age of both sexes, which is related to maternal variables. Older mothers have heavier offspring than do younger mothers, and higher-ranking mothers have heavier offspring than do lower ranking mothers. Mass advantages conferred upon offspring during lactation by older and higher-ranking mothers tend to persist postweaning in both sexes. Thus maternal factors affect reproductive success in both sexes, influencing the age at which offspring mature and begin their reproductive career.

Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx).

Previous studies of semifree-ranging mandrills identified two morphological and social variants of the adult male, based on behavioral and secondary sexual characteristics. "Fatted" males are social, with highly developed sex skin coloration, large testes, high plasma testosterone levels, and fat rumps; while "nonfatted" males are peripheral or solitary, with paler sex skin, smaller testes, lower plasma testosterone, and slimmer rumps. We present a detailed study of morphology and group association for 10 adult male mandrills, living in two semifree-ranging groups in Gabon, in order to relate differences between males to dominance rank. The results show that rather than existing as two distinct morphotypes, male mandrills represent a continuous spectrum of possibilities between social males with fully developed secondary sexual characteristics, and solitary males with muted secondary sexual characteristics. Alpha males (N = 2) had the highest testosterone levels, the most colorful sex skin, and the most active sternal glands, and were the only males to spend 100% of their time with the social group. Rank relationships between nonalpha males (N = 8) were not always clear, but all subordinate males had lower testosterone levels and less development of the secondary sexual adornments, and were less group-associated than alpha males. These findings suggest that only alpha males have sufficient testosterone to develop full secondary sexual characteristics, and we propose possible socioendocrine mechanisms underlying the suppression of testosterone and secondary sexual development in subordinate adults. We discuss differences in secondary sexual development in relation to reproductive strategies, and discuss the evolution of alternative reproductive morphs in primates.

Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status.

Two semifree-ranging mandrill groups, inhabiting large, naturally rainforested enclosures in Gabon, were studied to measure morphological, endocrine, and behavioral changes that occurred when adult males rose, or fell, in dominance rank. Gaining alpha rank (N = 4 males) resulted in increased testicular size and circulating testosterone, reddening of the sexual skin on the face and genitalia, and heightened secretion from the sternal cutaneous gland. Blue sexual skin coloration was unaffected. New alpha males increased in rump "fattedness," but not in body mass, and spent more time associated with other group members, rather than ranging alone. Loss of alpha position (N = 4 males) resulted in less pronounced effects than those that occurred after males had risen to alpha positions. Deposed alpha males showed decreased testicular volume, decreased body mass, a reduction in the extent of red (but not blue) sexual skin coloration, and decreased sternal gland activity. Deposed males did not decrease in the brightness of sex skin coloration. These results demonstrate that male-male competition and rank reversals have remarkable effects upon testicular function, secondary sexual traits, and behavior in the adult male mandrill. Secondary sexual traits respond to changes in male social status and therefore may be important as intrasexual signals of dominance rank.

Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx).

Male mandrills (Mandrillus sphinx) have spectacular secondary sexual adornments. These include red and blue sexual skin on the face, rump, and genitalia; a sternal scent-marking gland; and a "fatted" rump. Mandrills are seasonal breeders, and in other seasonally-breeding primate species members of both sexes may show increased expression of secondary sexual characteristics during the mating season. We examined changes in male secondary sexual adornments and testosterone levels, in relation to seasonal changes in the female reproductive cycle and sexual skin morphology, in two semifree-ranging mandrill groups. Females showed circannual changes in sexual skin tumescence, and periods of tumescence peaked from May-July in a long-established group. However, formation of a second, smaller group, two years previous to commencement of the study, disrupted the seasonal pattern of sexual skin tumescence and births. As the groups occupied adjacent enclosures, it appears that social factors, as well as physical environment, affected the seasonal patterning of reproduction in females. Male mandrills, by contrast, did not exhibit marked circannual changes in secondary sexual traits. Although adult male testicular volume and circulating testosterone levels increased significantly during the mating season, sexual skin coloration and rump "fattedness" showed no consistent changes with season. There was some evidence to suggest that maturing males (ages 5-8 yr) showed increased development of red sexual skin during mating periods, but once males had fully developed secondary sexual adornments, they remained stable throughout the year. The possible reasons for this are discussed in relation to intermale competition and social organization in mandrills.

Preliminary observations on sexual behavior and the mating system in free-ranging lesser galagos. (Galago moholi).

Sexual and associated patterns of behavior of lesser galagos (Galago moholi) were recorded during an 18-month study conducted at the Nylsvley Nature Reserve in South Africa. Animals were trapped and fitted with radio transmitter belts in order to monitor nocturnal activities during twice-yearly mating seasons. Most copulations occurred during the last week in May, while a subsidiary (post-partum) mating season occurred in late September-early October. Females came into estrus sequentially during the May season. Adult males exhibited increase in body weight and testes volume during the mating season, changes which were most pronounced among the larger males (> 226 g). Larger males also had the greatest mating success, initiating 88% of observed copulations. Sixty-seven percent of matings involved more than one male copulating with the same female during her estrus, which lasted 1-3 days. Mounts were prolonged (range 2-53 min, mean 9.0 min) and males copulated repeatedly (2-5 times) with the same partner during a single night. These observations of sexual behavior and of large relative testes size in free-ranging lesser galagos are consistent with the occurrence of a dispersed mating system involving sperm competition in this nocturnal prosimian species.

Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta).

In several primate species, males have been shown to exhibit a surge in circulating testosterone during the early postnatal period. This surge has been postulated to play a role in the development of sex differences in behavior. In this study, the role of postnatal testosterone in infant behavioral development was investigated in socially living rhesus macaques. Seven male infants were treated with a GnRH agonist, avorelin, from the first week of life onwards. Ten female infants were exposed to testosterone by implantation of capsules containing testosterone. The behavioral development of these and control infants was recorded from birth to 6 months of age. The sexually dimorphic patterns of play and mounting were not affected by manipulation of postnatal testosterone in either male or female infants. Similarly, most mother-infant interactions were not affected by the hormonal manipulation of infants. Mothers of testosterone-treated females were found to take more responsibility for moving into and out of arm's reach of their infants than mothers of some other groups of infants; however, this measure did not normally differ between mothers of male and female infants. Manipulation of the postnatal testosterone surge does significantly affect penile growth and development, but does not affect the expression of infant sex differences in behavior nor greatly affect the development of the mother-infant relationship in rhesus macaques.

Manipulation of postnatal testosterone levels affects phallic and clitoral development in infant rhesus monkeys.

Male primates exhibit marked elevation of circulating testosterone levels during the early postnatal period. The aim of this project was to test whether experimental manipulation of circulating testosterone levels in male and female infant rhesus monkeys affected development of the external genitalia during the first six months of life. Four groups of infants were studied. Seven control male infants exhibited high circulating testosterone levels during the first three months of life. Seven males were treated with a GnRH agonist (avorelin) from the first week of life onwards, which suppressed the postnatal testosterone surge. Ten control females exhibited low circulating testosterone levels during the early postnatal period. Administration of testosterone to 10 females resulted in high circulating levels in these infants. Fortnightly blood samples and genital measurements were taken from all infants during the first six months of life. Growth of the penis of avorelin-treated males was significantly retarded when compared to control males. Average length of the penis at six months of age was significantly (p = 0.012) smaller for avorelin-treated males (25.2 +/- 2.8 mm) than for control males (37.3 +/- 3.0 mm). Avorelin-treated males attained only around 50% detachment of the prepuce from the glans of the penis, while control males averaged 90% detachment. Treatment of females with testosterone resulted in significant growth of the clitoris in comparison to control females. The growth rates of the penis of control males and clitorides of testosterone-treated females were similar and greatest during the first two months of life. Gain in body weight was not affected by either hormonal manipulation. It is concluded that manipulation of circulating testosterone levels during the early postnatal period affects penile and clitoral development of infant rhesus monkeys. This postnatal period may therefore represent an important stage in penile development in primates.

The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta).

Observations were made on four captive breeding groups of rhesus monkeys in order to measure hormonal, behavioral, and genital changes in adolescent males during the annual mating season. Three questions were addressed with regard to possible effects of social environment upon reproductive maturation: (1) Does male agonistic rank influence adolescent development? (2) Does affiliation between adolescent males and adult females during the mating season influence the males' reproductive development? (3) Does maternal rank exert any effect upon reproductive maturation in adolescent sons? In many (but not all) cases male rank was positively correlated with circulating testosterone and testes weights during the mating season. Affiliative behavior (allogrooming and sexual interactions) between adolescents and adult females in their social groups bore no relationship to the degree of reproductive maturation in males. Mounts involving intromission were infrequent, but sons of high-ranking mothers gained significantly more intromissions than sons of lower-ranking females. Maternal rank was also found to correlate with circulating testosterone levels, testes weights, growth of the baculum (os penis), and maintenance of body weight in adolescent sons during the mating season. By contrast, levels of beta-endorphin in the cerebrospinal fluid of adolescent males did not correlate with social rank, testosterone levels, or genital development. These findings point to possible effects of maternal rank, as well as intermale agonistic rank, in determining reproductive maturation during adolescence in the male rhesus monkey.

Effects of altering testosterone in early infancy on social behaviour in captive yearling rhesus monkeys.

Thirteen male and twenty female rhesus monkeys (Macaca mulatta), aged 9-12 months, living as members of long term captive social groups, were observed in order to quantify sex differences in a variety of behaviour patterns. Six males had been treated with a GnRH agonist (Meterelin: M) during their first six postnatal months, in order to block the surge of testosterone which occurs at this time. Ten females had been treated with testosterone (T) during their first six months, in order to mimic the postnatal T surge seen in males. The remaining 7 males and 10 females acted as control subjects. Marked sex differences were measured in frequencies of play and socio-sexual behaviour in these juvenile monkeys. However, neither M nor T treatments produced any significant changes in frequencies of these behaviour patterns. Although M-treated males showed a tendency (p < 0.1) to groom others for longer periods than control males, and control females tended to spend more time alone than T-treated females, we were unable to measure any significant (p < 0.05) effects of either M- or T-treatment upon affiliative behaviour in juvenile rhesus monkeys. We conclude, therefore, that the postnatal T surge in male rhesus monkeys does not affect development of sexually dimorphic and associated patterns of behaviour. Presumably, organisational effects of T upon these behaviour patterns must be completed before birth in this species.

Sexual behavior, sexual swelling, and penile evolution in chimpanzees (Pan troglodytes).

Functional relationships between the penis, vagina, and cervix during copulation in the chimpanzee were studied. In 11 adult males, penile length during full erection ranged from 10.0-18.0 cm (mean +/- SD = 14.4 +/- 2.02). In 19 parous adult females examined during the early follicular phase of the cycle, or during lactation, vaginal depth (from the introitus to the os cervix) ranged from 9.8-16.5 cm (mean +/- SD = 12.6 +/- 1.69). However, when the sexual skin was maximally swollen, vaginal depth increased by up to 52% in some cases and ranged from 15.2-20.1 cm (mean +/- SD = 16.9 +/- 1.68). Under such conditions males vary in their ability to achieve maximal depth of intromission. Observations made on 6 females after natural matings revealed that in some cases males had deposited copulatory plugs in contact with the cervix, while in others plugs were lower down in the vagina. Direct observations under fluoroscopy using an artificial "penis" loaded with radio-opaque medium showed that the filiform tip can make contact with the os cervix. However, expulsion of radio-opaque medium under these conditions failed to demonstrate any immediate transfer of fluid through the cervix into the uterus. These studies indicate that, aside from its functions as a visual signal, the female chimpanzee's sexual skin swelling adds considerably to the distance males must negotiate during copulation to place spermatozoa at the cervical os. Evolution of the male's elongated, filiform penis may therefore be the result of sexual selection, to negotiate the long vagina of the female and to penetrate copulatory plugs deposited during previous copulations.

Sexual and aggressive behaviour of adult male marmosets (Callithrix jacchus) castrated neonatally, prepubertally, or in adulthood.

During early postnatal development, males of some primate species exhibit higher levels of plasma testosterone than females. The possible significance of this for behavioural development was examined in male marmosets castrated neonatally (NC), prepubertally (PC), or in adulthood (AC) and reared in their natal groups. Age-matched intact (AI) adult males served as controls. All males were removed from their natal groups as adults for pair testing with unfamiliar conspecific males and females. NC males did not mount, but were frequently aggressive during tests with females. NC males also elicited aggression from females but rarely from intact males. PC and AC males attempted copulation during the majority of tests with females; less aggression occurred but more so in tests with PC males than between females and AC males. Aggression between PC or AC males and intact males was much more frequent than when NC males met intacts in paired encounters. Results show that secretion of testicular hormones during infancy in male marmosets has important effects upon the development of sexual and aggressive behaviour. Castration in infancy has measurably different effects upon behavioural development than castration performed later in life (prepubertally or in adulthood).

Effects of testosterone propionate upon the sexual and aggressive behavior of adult male marmosets (Callithrix jacchus) castrated as neonates.

In New World monkeys of the family Callitrichidae (marmosets and tamarins), females frequently give birth to dizygotic twins. Twins share a placental circulation throughout fetal development and are hemopoietic chimeras. Despite this, there is no masculinization (freemartinism) in females which develop next to a male co-twin. It has been suggested that the organizing effects of testicular androgen upon sexual differentiation of the brain occur mainly during early postnatal development in male callitrichids, rather than in utero. However, this report demonstrates activation of masculine copulatory behavior by testosterone propionate (TP) administered to adult male marmosets (N = 8) which were castrated in infancy (between Days 1-7). Effects of neonatal castration upon aggressive behavior during pair tests with females (high frequencies of aggression) and intact adult males (low frequencies of aggression) were also reversed by TP treatment in adulthood. While early postnatal androgen secretion plays an important role in behavioral development in marmosets, it appears that a substantial degree of neural sexual differentiation occurs in utero in males of this callitrichid species.

Observations on effects of neonatal castration upon sexual and aggressive behavior in the male common marmoset (Callithrix jacchus).

The behavior of eight adult male marmosets that were bilaterally castrated during neonatal life (postnatal days 1-7), a single unilaterally castrated male, and eight age-matched intact adult males was observed during encounter tests with unfamiliar conspecifics. When neonatally castrated (NC) males encountered ovariectomized, estradiol-treated females, both partners were intensely aggressive and 66% of tests were terminated to avoid injuries. No mounts occurred, and females exhibited little or no sexual initiating behavior (proceptivity) towards NC males. By contrast, encounters between NC males and intact adult males were characterized by low levels of aggression and no tests were terminated. Intact males frequently mounted NC males. However, NC males initiated only 4% of these mounts by intact males and they refused or terminated 67% of mount attempts and mounts by intact males. The age-matched intact adult males provided data which differed markedly from those obtained using NC males. The intact males were highly aggressive during encounters with other intact males, whereas they mounted and ejaculated when paired with females. The single male which had been unilaterally castrated in infancy provided similar results to the intact males. These experiments indicate that neonatal castration has profound effects upon the development of sexual and aggressive behavior in male marmosets. However, the stimulus qualities as well as the behavior of males are altered by neonatal castration, so that unfamiliar conspecifics react towards them as females during paired encounters. This finding complicates the interpretation of effects of neonatal castration upon development of sexually dimorphic behavioral patterns in male marmosets. Behavioral effects of castration later in postnatal development romain to be determined. © 1993 Wiley-Liss, Inc.

Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx).

Positive correlations between dominance rank and plasma testosterone levels have been described for adult males of several primate species in captivity, but the relevance of such observations to free-ranging animals is unclear. CIRMF in Gabon maintains a breeding group of 45 mandrills in a six hectare, naturally rainforested enclosure. This study describes correlations between dominance rank (in agonistic encounters), levels of plasma testosterone, testicular volume, body weight, and development of secondary sexual characteristics (red and blue sexual skin on the muzzle and rump areas) in male mandrills under semifree ranging conditions. Two morphological and social variants of adult male mandrill were identified. Large-rumped or fatted adult males (n = 3) remained in the social group and exhibited maximal development of sexual skin coloration as well as large testicular size and highest plasma testosterone levels. By contrast, slimmer-rumped or nonfatted males (n = 3) lived a peripheral or solitary existence and these exhibited less development of their secondary sexual coloration and had smaller testes and lower plasma testosterone levels. Longitudinal studies of gonadal development in these six males revealed that testicular volumes and plasma testosterone levels increased most rapidly during pubertal development (4-5 years of age) in the three animals which proceeded to the fatted condition. These included the highest ranking, group-associated male which exhibited the most intense sexual skin coloration and had higher testosterone levels, although this was not correlated with testicular volume. This study shows that in the male mandrill social factors and reproductive development are interrelated.(ABSTRACT TRUNCATED AT 250 WORDS)

Development from birth to sexual maturity in a semi-free-ranging colony of mandrills (Mandrillus sphinx) in Gabon.

This report presents information collected over 7 years (1983-1990) in Gabon, on a breeding group of 14, increasing to 45, mandrills maintained in a rainforest enclosure. Under these conditions, a seasonal cycle of mating (June-October) and birth (January-May) occurred. Females began to exhibit sexual skin swellings at age 2.75-4.5 years (3.6 +/- 0.6 years, mean +/- SD; n = 10) and first delivered offspring when 3.25-5.5 years old (4.4 +/- 0.8 years; n = 9). Gestation periods ranged from 152 to 176 days (167 +/- 9 days; n = 6 accurately dated pregnancies) and interbirth intervals from 11 to 15 months (12.4 +/- 1.3 months; n = 15). Females could reproduce 2 years before attaining adult body weight (10-15 kg) and complete dental eruption by 5.0-5.5 years. Males, by contrast, developed more slowly, reaching adult body weight (30-35 kg) and testicular volume (volume of left testis: 25-30 ml) at 8 years. Consistently high circulating testosterone concentrations (8.17 +/- 2.0 ng ml-1) could be measured by 9 years of age. Fully developed males exhibited fatting of the rump and flanks, as well as striking sexual skin coloration and an active sternal cutaneous gland; little expression of these features was evident during pubertal development. Marked individual age differences occurred with regard to the onset and complete development of these features, suggesting possible interactions between social environment and physical maturation.