Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: implications for understanding developmental arrest

There are two morphs of reproductive male in orangutans. Both morphs span the age range from adolescent to adult, but "subadult" males are smaller in size and lack secondary sexual features. In this study, urine samples were collected over a 2 year period from 23 captive male orangutans in order to define the endocrinology of this apparent arrest of secondary sexual development. Three males were juveniles, 3 to 5 years of age; seven males showed no secondary sexual trait development and were over 7 years of age; six males were in the process of developing secondary sexual features, with the youngest male being 6 years of age; and seven males were fully mature adults. Morning samples were analyzed by radioimmunoassay for levels of growth hormone (GH) and thyroid-stimulating hormone (TSH) and group hormone profiles were compared by analysis of variance. GH is the primary hormone of growth and development and its increase in teenage boys is associated with the adolescent growth spurt. TSH stimulates the thyroid to produce and secrete hormones that have metabolic effects and required for normal growth and development. Results show that arrested adolescent male orangutans have a GH level about 1/3 that of developing adolescents (P = .0006). TSH levels do not differ significantly between arrested and developing adolescents. These data complement other endocrine data showing significantly lower levels of sex steroids and luteinizing hormone (LH) in arrested males than developing males [Maggioncalda, 1995a,b; Maggioncalda et al., 1999]. Together with documented behavioral differences between reproductive males with and without secondary sexual features, these endocrine data support the hypothesis that in male orangutans there are alternative developmental pathways and corresponding alternative reproductive strategies.     

Reproductive hormone profiles in captive male orangutans: Implications for understanding developmental arrest

For many years researchers have described some male orangutans as “subadult.” These males are of adolescent to adult age and are reproductive, but have little to no secondary sexual trait development. Until now the only endocrine study of this arrest of secondary sexual trait development was performed by Kingsley (1982, 1988). She found that “subadult” or arrested males have lower testosterone levels than similar age developing adolescents or adult males. In this study, urine samples were collected over a two-year period from 23 captive male orangutans in order to more fully define male endocrine profiles. Three study males were juveniles, seven were arrested adolescents, six were developing adolescents, and seven were mature adults. Morning samples were analyzed by radioimmunoassay for levels of testicular steroids and gonadotropins and group hormone profiles were compared by analysis of variance. Results illustrate that arrested adolescent orangutans have significantly lower testosterone and dihydrotestosterone (DHT) levels than developing adolescents, but significantly higher levels than juveniles. Luteinizing hormone (LH) levels also differed between arrested and developing adolescents, with arrested males having lower levels. However, follicle stimulating hormone (FSH) levels were similar in both morphs of adolescent male. The overall hormone profiles for arrested and developing adolescent male orangutans suggest that arrested males lack levels of LH, testosterone, and DHT necessary for development of secondary sexual traits. However, they have sufficient testicular steroids, LH, and FSH to fully develop primary sexual function and fertility. These endocrine data help define alternative developmental pathways in male orangutans. The authors discuss the relationship between these developmental pathways and male orangutan reproductive strategies, and hypothesize about their prepubertal socioendocrine determination. Am J Phys Anthropol 109:19–32, 1999. © 1999 Wiley-Liss, Inc.     

Male orangutan subadulthood: a new twist on the relationship between chronic stress and developmental arrest

Both in the wild and in captivity, a marked and enduring arrest of secondary sexual developmental occurs in some male orangutans (Pongo pygmaeus) (Kingsley [1982] The Orang-Utan: Its Biology and Conservation, The Hague: Junk; Utami [2000]). Researchers have hypothesized that chronic stress, perhaps related to aggression from mature males, causes endocrine changes altering growth and maturation rates in these males (Maple [1980] Orangutan Behavior, New York: Van Nostrand Reinhold; Graham [1988] Orangutan Biology, Oxford: Oxford University Press). In this study, urine samples were collected over a 3-year period from 23 captive male orangutans to test the hypothesis that developmentally arrested male orangutans have an endocrine profile consistent with chronic stress. Three study males were juveniles, seven were arrested adolescents, six were developing adolescents, and seven were mature adults. Morning samples were analyzed by radioimmunoassay for levels of the stress hormones cortisol and prolactin, and group hormone profiles were compared by analysis of variance. Results indicate that developing adolescent male orangutans have a significantly higher stress hormone profile than juvenile, developmentally arrested adolescent, or adult males. These results imply that the arrest of secondary sexual development in some male orangutans is not stress-induced, but instead perhaps an adaptation for stress avoidance during the adolescent or "subadult" period. These data, together with previously reported data on levels of gonadotropins, testicular steroids, and growth-related hormones, define endocrine profiles associated with alternative reproductive strategies for males with and males without secondary sexual features (Maggioncalda et al. [1999], [2000].     

Changes in social interactions during adolescence in male mandrills (Mandrillus sphinx)

The adolescent period in male mandrills extends from the time the testicles descend (at the age of 3-4 years) to the time adult characteristics develop (at the age of 10 years), and is thus one of the longest adolescent periods in cercopithecines. In this short cross-sectional study of 11 male mandrills (4.7-9.1 years old), we analyzed social behavioral patterns to investigate partner preference and changes in types of interactions throughout puberty. The mandrills were separated into two clusters on the basis of all of the social interactions scored, as well as the age and sex of the protagonist. During early to mid puberty, immature individuals interacted preferentially with other male adolescents and juveniles. Playing was an important activity, and some affiliative interactions with juveniles were observed. Older adolescents interacted more with adult males and females. These older adolescents were predominantly aggressive toward other adolescents, females, and juveniles, and showed little or no affiliative or playful behaviors. These results indicate a shift in social partners: older males interacted more frequently with adult males, and their behavior involved more aggression and less submission compared to younger adolescents, which showed predominantly submissive and playful behavior. These changes are consistent with preparation for dispersal and future intermale competition.     

Does Breeding Ornamentation Signal Genetic Quality in Arctic charr, <Emphasis Type="Italic">Salvelinus alpinus</Emphasis>?

Genetic theories of sexual selection predict that most ornamental secondary sexual traits provide reliable indication of the genetic quality of their bearers. Accordingly, also the offspring of mates with elaborate mating display should perform better than those of less conspicuous counterparts. In this study, we used Arctic charr (Salvelinus alpinus) as a model species to investigate whether the variation in a carotenoid-based red breeding coloration (a sexually dichromatic trait) in different sexes would reflect differences in individual genetic variability, one measure of individual quality, and/or indirectly, be manifested in variation in the offspring’s early viability and growth. We created maternal half-sibling families by artificially fertilizing the eggs with milt from bright- and pale-coloured males and then held the resulting progenies under identical hatchery conditions. The expression of red coloration among parental fish was not associated with their genetic diversity estimates in either sex nor did offspring sired by bright males consistently differ in terms of embryo survival or endogenous growth efficiency from offspring sired by pale males. By contrast, maternal effects were notably strong and, additionally, the degree of female coloration was negatively linked to their reproductive potential. The more intensely coloured females had a smaller relative fecundity and they also produced offspring of lower viability, implying a significant trade-off in resource allocation between ornamentation and offspring. Our results indicate that the red breeding ornamentation of Arctic charr is likely to be informative rather among females than males when the reproductive quality is predicted on grounds of the number of offspring produced. Nevertheless, this study does not support the direct selection hypothesis in explaining the evolution of female ornamentation, but rather suggests that the less intense coloration of female charr compared to males may reflect inter-sexual differences in the trade-off between natural and sexual selection.     

Sex-limited mutations and the evolution of sexual dimorphism

Abstract.— Although the developmental and genetic mechanisms underlying sex differences are being elucidated in great detail in a number of species, there remains a breach between proximate and evolutionary studies of sexual dimorphism. More precisely, the evolution of sex-limited gene expression at autosomal loci has not been well reasoned using either theoretical or empirical methods. Here, I show that a Mendelian genetic model including elementary details of sexual differentiation provides novel insight into the evolution of sex differences via sex limitation. This model indicates that the nature of allelic effects and the pattern of selection must be known in both sexes to predict the evolution of sex differences. That is, selection interacts with genetic variation for sexual dimorphism to produce unanticipated patterns of trait divergence or convergence between the sexes. Ultimately, this model may explain why previous models for the evolution of sexual dimorphism do not predict the erratic behavior of the sex difference during artificial selection experiments.     

Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata)

Behavioral observations on juvenile mantled howlers are limited by visually undifferentiated genitalia; however, animals can be sexed when they are very young or if they are captured. Behavioral data and fecal samples from juveniles during month-long field studies from 1993 to 1995 were analyzed to determine whether there are developmental differences in behavior or hormone concentrations that can be used to differentiate males from females. The subjects were juveniles of known sex and age from five different social groups on Hacienda La Pacifica, Costa Rica. Based on 749.8 hr of focal-animal sampling, there were no sex differences in daily activity patterns. There were no sex differences in proximity to mothers and other group members, and age differences reflected howler life-history patterns. There were no differences in estradiol or testosterone concentration by age or sex. Juvenile monomorphy thus extends beyond morphology to behavioral and hormonal similarity as well. Most juveniles are forced out of their natal groups and remain solitary until they join new groups by supplanting all same-sex adult group members. Monomorphy may allow them to spend more time in natal groups, and thus both reduce the solitary period and allow the juveniles to improve social skills needed for later immigration. While this strategy may benefit juvenile howlers, it remains a problem for those who wish to study juvenile sex differences from a distance.     

The Influence of the Family on Adolescent Sexual Experience: A Comparison between Baltimore and Johannesburg

The main objective of this paper is to understand the role of the family on the sexual experiences of adolescents from urban, disadvantaged settings in Baltimore and Johannesburg. Data were collected as part of the WAVE study, a global study of disadvantaged youth in five cities. Qualitative data were based on key informant interviews, a Photovoice exercise, community mapping, focus groups and in-depth interviews with adolescents. Quantitative data were gathered from an ACASI survey that was administered to approximately 450–500 adolescents per site. Results from the qualitative data revealed that while parents were viewed as important sources of information for sexual and reproductive health, they were often not present in the adolescents’ lives. This lack of parental presence was perceived to result in adolescents feeling an overall lack of adult support and guidance. The impact of parental presence and support on adolescent sexual experience was further examined from the quantitative data and revealed a complex picture. In both Baltimore and Johannesburg, female adolescents who were raised by other relatives were less likely to report having had sex compared to those raised by two biological parents, which was not observed for males. In Johannesburg, female adolescents who were paternal orphans were less likely to have had sex compared to non-orphans; the opposite was true among males. Finally, in both sites, female adolescents who had been exposed to violence were more likely to have had sex compared to those who had not; for males, there was no significant relationship. The study demonstrates the powerful influence of both context and gender for understanding the influences of the family on adolescent sexual behaviors. Programs aiming to reduce adolescent sexual risk behaviors the need to understand the complex influences on risk behaviors in different settings and in particular, the role of mothers and fathers. Prevention strategies need to also understand and incorporate gender-specific messages and interventions in order to address the high risk of sexual behaviors among adolescents in these settings.     

The Number of Louse Eggs on Wild Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) Varies with Age,but Not with Sex or Season

During grooming, primates remove harmful ectoparasites, such as ticks and lice, and there is direct evidence for a health benefit of tick removal. Grooming behaviors differ among primates with respect to age and sex. Moreover, the number of ectoparasite may exhibit seasonal variation. Therefore the number of ectoparasites on a host may vary with effects, host age and sex, and season. However, these effects have not been a focus of louse infestation studies of primates. Grooming in Japanese macaques is related to sex and age, with developmental changes in behavior corresponding to the timing of tooth eruption. Moreover, behavioral data for Japanese macaques suggest that lice load may differ with the season. Thus, we examined whether the number of louse eggs varies according to host macaque sex, age, and season, and whether it changes in response to tooth eruption. We counted unhatched and hatched eggs attached to the hair on six 1-cm² areas on the left wrist skin of culled macaques, using a stereoscopic microscope. We sampled five winter coats and three summer coats for each age class: infant, juvenile, adolescent, and adult. The number of unhatched and hatched eggs was related to age, but not to sex and season. There were significant differences in the number of unhatched eggs between infants and adults, juveniles and adults, and adolescents and adults. There were also significant differences in the number of hatched eggs between infants and adults, juveniles and adults, adolescents and adults. Tooth eruption did not influence the number of louse eggs. These results suggest that researchers should consider the age of host animals when assessing the relationship between grooming and ectoparasites.     

Differences in Subadult Behaviors of Chimpanzees Living in Peer Groups and in a Family Group

In several primate species, peer-group rearing conditions affect the development of social behavior. We compared the social behavior of adolescent chimpanzees reared in peer groups and in a family group to see whether chimpanzees raised under different regimes show differences in sexual behavior, teasing behavior, and grooming behavior and in their ability to cope with support strategies. Surprisingly, the lack of opportunity to practice or to watch in peer groups had no measurable effect on the development of normal sexual behavior in adolescence and adulthood. Peer-group individuals groomed each other as much as peers did in the zoo. Sex differentiation in reaction to teasing and in conflict initiatives may indicate only an earlier sex differentiation in the zoo than in the peer group. This result may be attributed to the difference in demographic composition of the groups instead of some inherent difference in skill. Peer-group chimpanzees simply cannot find adult partners with which they may preferably test their position. However, there was a lack of sex differentiation in the reaction to teasing and in the number of conflicts started; both are indications of lesser sex-role development in the peer-group adolescents. Furthermore, the frequency of giving support to peers in conflicts differed, which suggests a greater ability in zoo adolescents to cope with support strategies. Accordingly, providing more natural conditions than is usual in laboratories may still add considerably to chimpanzee well-being.     

Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards

The evolution of conspicuous male display ornaments is a common trend in diverse groups of organisms and a continuing challenge to studies of sexual selection. A phylogenetic approach was used to examine macro-evolutionary patterns of change in sexually dichromatic display coloration (distinctively coloured belly patches) among 130 taxa of phrynosomatid lizards. The results showed repeated losses of sexual dimorphism, which occur through losses of conspicuous male coloration or gains of conspicuous female coloration. The frequent loss of male traits is surprising, given that sexual selection presumably drives their evolutionary origin and maintenance, but is consistent with a recently proposed hypothesis suggesting that females may lose responsiveness to male traits over macro-evolutionary time-scales. The observation of repeated losses of male traits in phrynosomatid lizards (and other groups) may have implications for testing among competing models for the evolution of female preferences. A concentrated changes test showed that changes in male display coloration are significantly associated with the use of ground-dwelling habitat, as opposed to rock- or tree-dwelling habitats. This result suggests a role for natural selection in the loss of male display traits in phrynosomatid lizards, but habitat type alone may be insufficient to explain these losses.     

Are age and sex differences in brain oxytocin receptors related to maternal and infanticidal behavior in naïve mice?

This article is part of a Special Issue “Parental Care”.There is significant variability in the behavioral responses displayed by naïve young and adult mice when first exposed to pups. This variability has been associated with differences in the expression of oxytocin receptors (OXTRs) in the brain in several species. Experiment I investigated the behavioral responses of juvenile, adolescent, and adult CB57BL/6 males and females when first exposed to pups. We found an age increase in maternal females (11% of juveniles, 20% of adolescents, and 50% of young adults), and infanticidal males (0% of juveniles, 30% of adolescents, 44.5% of young adults, and 100% of older adults). Experiment II investigated OXTR density in the brain of juvenile and adult mice. Our results revealed an age decline in the density of OXTR in several brain regions, including the lateral septum, cingulated and posterior paraventricular thalamic nucleus in both males and females. Adult females had higher OXTR density in the ventromedial nucleus/postero-ventral hypothalamus (VMH) and the accessory olfactory bulb (AOB), but lower density in the ventral region of the lateral septum (LSv) than juveniles. Males had lower OXTR density in the anterior olfactory area (AOA) compared to juveniles. No age or sex differences were found in the medial preoptic area, and amygdaloid nuclei, among other brain regions. This study suggests that 1) maturation of parental and infanticidal behavioral responses is not reached until adulthood; 2) the pattern of development of OXTR in the mouse brain is unique, region specific, and differs from that observed in other rodents; 3) either up or down regulation of OXTR in a few brain regions (VMH/AOB/LSv/AOA) might contribute to age or sex differences in parental or infanticidal behavior.     

Sex differences in mortality of Japanese macaques: Twenty-one years of data from the Arashiyama West population

Theorists argue that mortality in male mammals should be higher than that of females, and many studies of primates followed across the life course have found this to be the case. This study examines mortality patterns in the rapidly expanding Arashiyama West (Texas) population of Japanese macaques (Macaca fuscata) and finds that males have a significantly lower median survival age (12.2 years) in comparison to females (20.5 years). Males and females are born in equal proportions, but by adulthood there are 2–5 females to every male. Males are at higher risk of falling victim to infectious diseases and human-related causes of death, and they are more likely to “disappear” from the population, which is inferred to result largely from emigration. There are no significant sex differences in the risks of dying from predation, non-infectious illnesses, neonatal defect, or social stress. Males become more susceptible to mortality than females once they reach sexual maturity, and they remain at greater risk than females until their old age. There is no evidence that one sex or the other is at greater risk of dying as infants, or as juveniles. Comparing males of different age classes, adolescent and adult males are more likely to die and to disappear than are juvenile males. These findings support the “high-risk, high-gain” hypothesis that males are mainly lost to the population because of their risk-taking behaviors after sexual maturity, rather than the “fragile male” hypothesis that males are more vulnerable to mortality during the period of growth and development. Am J Phys Anthropol 102:161–175, 1997 © 1997 Wiley-Liss, Inc.     

Lower extremity control during turns initiated with and without hip external rotation

The pirouette turn is often initiated in neutral and externally rotated hip positions by dancers. This provides an opportunity to investigate how dancers satisfy the same mechanical objectives at the whole-body level when using different leg kinematics. The purpose of this study was to compare lower extremity control strategies during the turn initiation phase of pirouettes performed with and without hip external rotation. Skilled dancers (n=5) performed pirouette turns with and without hip external rotation. Joint kinetics during turn initiation were determined for both legs using ground reaction forces (GRFs) and segment kinematics. Hip muscle activations were monitored using electromyography. Using probability-based statistical methods, variables were compared across turn conditions as a group and within-dancer. Despite differences in GRFs and impulse generation between turn conditions, at least 90% of each GRF was aligned with the respective leg plane. A majority of the net joint moments at the ankle, knee, and hip acted about an axis perpendicular to the leg plane. However, differences in shank alignment relative to the leg plane affected the distribution of the knee net joint moment when represented with respect to the shank versus the thigh. During the initiation of both turns, most participants used ankle plantar flexor moments, knee extensor moments, flexor and abductor moments at the push leg׳s hip, and extensor and abductor moments at the turn leg׳s hip. Representation of joint kinetics using multiple reference systems assisted in understanding control priorities.     

Meloxicam Blocks Neuroinflammation,but Not Depressive-Like Behaviors,in HIV-1 Transgenic Female Rats

Adolescents living with human immunodeficiency virus (HIV) comprise approximately 12% of the HIV-positive population worldwide. HIV-positive adolescents experience a higher rate of clinical depression, a greater risk of sexual and drug abuse behaviors, and a decreased adherence to highly active antiretroviral therapies (HAART). Using adolescent HIV-1 transgenic rats (HIV-1 tg) that display related immune response alterations and pathologies, this study tested the hypothesis that developmental expression of HIV-1-related proteins induces a depressive-like phenotype that parallels a decrease in hippocampal cell proliferation and an increase in pro-inflammatory cytokine expression in the hippocampus. Consistent with this hypothesis, adolescent HIV-1 tg rats demonstrated a depressive-like behavioral phenotype, had decreased levels of cell proliferation, and exhibited elevated expression of monocyte chemotactic protein-1 (Mcp-1) in the hippocampus relative to controls. Subsequently, we tested the ability of meloxicam, a selective COX-2 inhibitor, to attenuate behavioral deficits via inflammatory mechanisms. Daily meloxicam treatments did not alter the behavioral profile despite effectively reducing hippocampal inflammatory gene expression. Together, these data support a biological basis for the co-morbid manifestation of depression in HIV-positive patients as early as in adolescence and suggest that modifications in behavior manifest independent of inflammatory activity in the hippocampus.     

Sex differences in giraffe foraging behavior at two spatial scales

We test predictions about differences in the foraging behaviors of male and female giraffes (Giraffa camelopardalis tippelskirchi Matchie) that derive from a hypothesis linking sexual size dimorphism to foraging behavior. This body-size hypothesis predicts that males will exhibit specific behaviors that increase their dry-matter intake rate relative to females. Foraging behavior was examined at two hierarchical levels corresponding to two spatial and temporal scales, within patches and within habitats. Patches are defined as individual trees or shrubs and habitats are defined as collections of patches within plant communities. Males were predicted to increase dry-matter intake rate within patches by taking larger bites, cropping bites more quickly, chewing less, and chewing faster. Within habitats, males were expected to increase intake rate by increasing the proportion of foraging time devoted to food ingestion as opposed to inter-patch travel time and vigilance. The predictions were tested in a free-ranging population of giraffes in Mikumi National Park, Tanzania. Males spent less total time foraging than females but allocated a greater proportion of their foraging time to forage ingestion as opposed to travel between patches. There was no sex difference in rumination time but males spent more time in activities other than foraging and rumination, such as walking. Within patches, males took larger bites than females, but females cropped bites more quickly and chewed faster. Males had longer per-bite handling times than females but had shorter handling times per gram of intake. Within habitats, males had longer average patch residence times but there was no significant sex difference in inter-patch travel times. There was no overall difference between sexes in vigilance while foraging, although there were significant sex by habitat and sex by season interactions. Although not all the predictions were confirmed, overall the results agree qualitatively with the body-size hypothesis. Sex-related differences in foraging behavior led to greater estimated intake rates for males at the within-patch and within-habitat scales. Received: 20 November 1995 / Accepted: 5 November 1996     

Selection in a fluctuating environment and the evolution of sexual dimorphism in the seed beetle Callosobruchus maculatus

Temperature changes in the environment, which realistically include environmental fluctuations, can create both plastic and evolutionary responses of traits. Sexes might differ in either or both of these responses for homologous traits, which in turn has consequences for sexual dimorphism and its evolution. Here, we investigate both immediate changes in and the evolution of sexual dimorphism in response to a changing environment (with and without fluctuations) using the seed beetle Callosobruchus maculatus. We investigate sex differences in plasticity and also the genetic architecture of body mass and developmental time dimorphism to test two existing hypotheses on sex differences in plasticity (adaptive canalization hypothesis and condition dependence hypothesis). We found a decreased sexual size dimorphism in higher temperature and that females responded more plastically than males, supporting the condition dependence hypothesis. However, selection in a fluctuating environment altered sex-specific patterns of genetic and environmental variation, indicating support for the adaptive canalization hypothesis. Genetic correlations between sexes (r(MF) ) were affected by fluctuating selection, suggesting facilitated independent evolution of the sexes. Thus, the selective past of a population is highly important for the understanding of the evolutionary dynamics of sexual dimorphism.     

Sexual segregation in childhood: a review of evidence for two hypotheses

In this paper, I review the evidence associated with two hypotheses, both ultimately derived from sexual selection theory, put forth to explain social sexual segregation in human juveniles. More proximately, I posit that segregation is motivated by sex differences in body size, physical activity and competitiveness. The first hypothesis, the energetic/behavioural hypothesis, suggests that difference in energetics is a way in which males differentiate themselves from females and develop muscle and brain systems implicated in reproductive roles. The second hypothesis, the social roles hypothesis, suggests that segregation is related to learning male and female reproductive roles. The reviewed evidence supports the view that there are differences in energetics in male and female groups. With development, the vigorous behaviours shown by males take the form of specific social roles, related to dominance and competitiveness for males and maternal roles for females.     

Female sexual swellings in the Asian colobine Simias concolor

During a preliminary study of pig-tailed langurs (Simias concolor) in the Pagai Islands, Indonesia, it was discovered that females exhibited conspicuous swelling of the urogenital triangle. The pig-tailed langur is the first Asiatic colobine found to have prominent sexual swellings and the only colobine with sexual swellings that lives in one-male groups. Because all anthropoids with conspicuous sex skin typically live in groups having female-biased adult sex ratios, it is possible that females might compete amongst themselves for the male in one-male groups, or the best males in multimale groups. Sexual swellings may therefore have resulted from sexual selection for signals attractive to males in female-female competition, as suggested earlier by Bercovitch (California Anthropologist 8:9–12, 1978). Prolonged observation of recognizable individuals will be required to test this hypothesis in the pig-tailed langur and other species.