Advances in human oxytocin measurement: challenges and proposed solutions.

Oxytocin, a neuropeptide known for its role in reproduction and socioemotional processes, may hold promise as a therapeutic agent in treating social impairments in patient populations. However, research has yet to uncover precisely how to manipulate this system for clinical benefit. Moreover, inconsistent use of standardized and validated oxytocin measurement methodologies-including the design and study of hormone secretion and biochemical assays-present unresolved challenges. Human studies measuring peripheral (i.e., in plasma, saliva, or urine) or central (i.e., in cerebrospinal fluid) oxytocin concentrations have involved very diverse methods, including the use of different assay techniques, further compounding this problem. In the present review, we describe the scientific value in measuring human endogenous oxytocin concentrations, common issues in biochemical analysis and study design that researchers face when doing so, and our recommendations for improving studies using valid and reliable methodologies.

Timing of the luteal-placental shift is delayed with additional fetuses in litter-bearing callitrichid monkeys, Saguinus oedipus and Callithrix jacchus.

The luteal-placental shift is an important milestone of mammalian pregnancy signifying when endocrine control of pregnancy shifts from the corpus luteum of the ovary to the placenta. The corpus luteum is maintained by chorionic gonadotropin (CG). Upon sufficient placental maturation, CG production wanes, the corpus luteum involutes, and control is shifted to the placenta, one consequence of which is a midgestational rise in glucocorticoid production, especially cortisol and cortisone, by both mother and fetus. Glucocorticoids are involved in initiating parturition, prenatal programming of offspring phenotype, and maturing fetal organs. Limited evidence from human pregnancy suggests that the timing of this shift is delayed in twin pregnancies, but little is known about the timing of the luteal-placental shift in litter-bearing monkeys from the primate family Callitrichidae. Here we provide evidence from cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus) of longer duration of elevated CG associated with multiple infant births compared to single births. Urinary profiles from cotton-top tamarins demonstrate that the decline of the extended elevation of CG precedes the onset of the midpregnancy sustained rise in glucocorticoids; this shift occurs later with an increase from one to two fetuses carried to term. In the common marmoset, the onset of the sustained rise of glucocorticoids in maternal urine is also delayed with an increase in infant number. Total urinary glucocorticoid levels during the last half of gestation increase monthly but do not differ by infant number. The significant delay in the luteal-placental shift suggests a longer period of placental maturation is needed to support a greater number of fetuses.

Cognitive development from infancy to young adulthood in common marmosets (Callithrix jacchus): Effect of age, sex, and hormones on learning and affective state.

Studies looking at individual variability in cognition have increased in recent years. We followed 43 marmosets (21 males, 22 females) from infancy to young adulthood. At 3-months old, marmosets were trained to touch a rewarded stimulus. At 9-, 15-, and 21-months old, they were given visual discrimination and cognitive bias tests, and urine samples were collected to examine hormone levels. Marmosets were significantly more successful learners at 15 months than 9 months. Individuals who were more successful learners at 9 months were also more successful at 15 months, with more male learners than expected at 15 months. At 9 months, learning success was associated with higher cortisol levels. At 15 months, males with higher estradiol levels were more successful learners, whereas at 21 months, females with higher estradiol and cortisol levels tended to be less successful learners and more pessimistic. Nine months, therefore, appears to be an important developmental timepoint for acquiring cognitive control, which has developed by 15 months. Steroids may have differential effects on each sex, with complex interactions between gonadal and adrenal hormones having an influence on cognitive function over the lifespan. This longitudinal study offers new insight into cognition, including its development and biological underpinnings.

Motivational increase of androgens and behavior by infant distress calls in highly responsive common marmoset fathers, Callithrix jacchus.

Common marmoset fathers are highly involved in care of their infants. However, variability exists in their response to infant behavior even in paternally experienced fathers. Using infant distress cries as a motivation test, we investigated: 1. the differences in paternally experienced fathers' motivation to search for the infant vocalization stimuli; 2. the relationship between a father's motivation to search for the source of the infant cries and testosterone levels; and 3. if there is a rapid steroidogenesis pathway leading to increased testosterone and estradiol in the peripheral circulation. Only 44% of the paternally experienced fathers showed a high frequency of searching for the source of the infant distress cries. Through the use of multisteroid analysis, we found high responsive fathers had significantly higher levels of progesterone and testosterone in response to infant distress cries compared to a control stimulus with progesterone and androstenedione correlating with testosterone, while no differences were seen in low responders. The frequency to search for the infant stimuli was positively correlated with higher testosterone compared to control vocal levels. These results suggest that searching for the source of infant cries represents a motivation behavior for fathers that is activated by testosterone and reflects rapid circulating testosterone.

Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy.

Behavioral observations can provide clues about female reproductive status. However, the study of the endocrine dynamics that underlie processes such as puberty, ovulation, conception, and gestation, may help increase our understanding of female reproductive biology. We used noninvasive methods to study female reproductive endocrinology in wild woolly monkeys (genus Lagothrix). We extracted ovarian steroid hormones from fecal samples collected non-invasively to examine changes in the concentrations of progesterone and estrogen metabolites (pregnanediol-3-glucuronide and estrone-3-glucuronide, respectively) during periods of female puberty, ovarian cyclicity, and pregnancy. The two subadult females in our study showed significant increases in ovarian hormone concentrations before disappearing and presumably dispersing, suggesting that they might reach the onset of puberty before emigrating from their natal groups. Ovarian cycle length in adult females was, on average, ~22 days (N = 21). Of the 10 cycling females, five conceived and four gave birth to offspring, with an average gestation period of ~214 days, but the infant born to the female with the shortest estimated gestation period (182 days) disappeared within a month after parturition. The fact that less than half of all cycling females conceived, and that only three out of five of those females gave birth to offspring that survived past the first month, suggests that reproduction is energetically costly for female woolly monkeys. Ovarian cycle length and gestation period among woolly monkeys are similar to those in their closest relatives, spider monkeys and muriquis suggesting that reproductive physiology may be highly conserved among females within the Tribe Atelini.

Contextual complexity of chemical signals in callitrichids.

In nearly four decades our research and that of others on chemical signaling in callitrichid primates suggest a high degree of contextual complexity in both the use of signals and the response to these signals. We describe our research including observational field studies, behavioral bioassays ("playbacks"), functional imaging, and conditioning studies. Scent marking in both captivity and the wild is used for more than just territorial marking. Social contextual effects are seen in responses by subordinate females responding with ovulatory inhibition only to chemical signals from familiar dominant reproductive females. Males detect ovulation through changes in scent marks. Males responded behaviorally and hormonally to chemical signals of novel ovulating females as a function of their reproductive status (fathers, males paired with a female but not fathers, and single males). Multiple brain areas are activated in males by female chemical signals of ovulation including areas relating to memory, evaluation, and motivation. Furthermore, males can be conditioned to respond sexually to a nonsexual odor demonstrating that learning plays an important role in response to chemical signals. Male androgen and estrone levels changed significantly in response to infant chemical signals as a function of whether the males were fathers or not, whether the odors were from their own versus other infants, as well as the infant's stage of development. Chemical signals in callitrichids are providing a rich source of understanding the context and function of the chemical sensory system and its stimulation of neural, behavioral, and hormonal actions in the recipients.

Early learning in the common marmoset (Callithrix jacchus): Behavior in the family group is related to preadolescent cognitive performance.

Early environment can have a major impact on development, with family life known to play an important role. Longitudinal studies can therefore help increase our understanding of variance in cognitive abilities in young animals, as well as over time. We followed 22 marmosets (11 male and 11 female) from infancy through to early adolescence. At 3 months old, the marmosets were trained to reliably touch a rewarded stimulus. At 5 months, behavior was observed within the natal group. At 9 months, the marmosets were given a visual discrimination task to assess learning ability. Mann-Whitney U tests found no sex or family size differences in number of errors at 3 or 9 months. While no significant relationships were found between behavior in the family and learning at 3 months, significant negative correlations were found between duration spent in locomotion and learning errors (p = .05), as well as between frequency of calm vocalizations and learning errors (p = .001) at 9 months. A U-shape curve was found between amount of social play and learning at 9 months. Positive family interactions, including moderate amounts of play, as well as calm individual behavior, may therefore be important in learning. This study sheds light on cognitive development in much younger marmosets than previously studied, and helps increase understanding of how individual differences in learning may arise.

Evaluation of vitamin D3 metabolites in Callithrix jacchus (common marmoset).

Vitamin D3 (cholecalciferol) is endogenously produced in the skin of primates when exposed to the appropriate wavelengths of ultraviolet light (UV-B). Common marmosets (Callithrix jacchus) maintained indoors require dietary provision of vitamin D3 due to lack of sunlight exposure. The minimum dietary vitamin D3 requirement and the maximum amount of vitamin D3 that can be metabolized by marmosets is unknown. Observations of metabolic bone disease and gastrointestinal malabsorption have led to wide variation in dietary vitamin D3 provision amongst research institutions, with resulting variation in circulating 25-hydroxyvitamin D3 (25(OH)D3 ), the accepted marker for vitamin D sufficiency/deficiency. Multiple studies have reported serum 25(OH)D3 in captive marmosets, but 25(OH)D3 is not the final product of vitamin D3 metabolism. In addition to serum 25(OH)D3, we measured the most physiologically active metabolite, 1,25-dihydroxyvitamin D3 (1,25(OH)2 D3 ), and the less well understood metabolite, 24,25-dihydroxyvitamin D3 (24,25(OH)2 D3 ) to characterize the marmoset's ability to metabolize dietary vitamin D3 . We present vitamin D3 metabolite and related serum chemistry value colony reference ranges in marmosets provided diets with 26,367 (Colony A, N = 113) or 8,888 (Colony B, N = 52) international units (IU) of dietary vitamin D3 per kilogram of dry matter. Colony A marmosets had higher serum 25(OH)D3 (426 ng/ml [SD 200] vs. 215 ng/ml [SD 113]) and 24,25(OH)2 D3 (53 ng/ml [SD 35] vs. 7 ng/ml [SD 5]). There was no difference in serum 1,25(OH)2 D3 between the colonies. Serum 1,25(OH)2 D3 increased and 25(OH)D3 decreased with age, but the effect was weak. Marmosets tightly regulate metabolism of dietary vitamin D3 into the active metabolite 1,25(OH)2 D3 ; excess 25(OH)D3 is metabolized into 24,25(OH)2 D3 . This ability explains the tolerance of high levels of dietary vitamin D3 by marmosets, however, our data suggest that these high dietary levels are not required.

From the field to the lab: Muriqui endocrinology from a collaborative perspective.

The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.

Measuring peripheral oxytocin and vasopressin in nonhuman primates.

Studying the neural and hormonal changes that modulate behavior is critical to understanding social relationships. Of particular interest is measuring oxytocin (OT) and arginine vasopressin (AVP) peripherally, and preferably, non-invasively, in nonhuman primates. Due to these peptides' neural origin and their stimulation of brain areas that influence social behavior, there has been debate whether peripheral measures in blood, urine, and saliva reflect central levels in the brain. This review elucidates the challenges of OT measurement and the solutions that provide valuable data on OT's role in social behavior. This review discusses the recent studies in rhesus macaques which indicate that exogenous OT delivered by nasal spray results in increased OT in cerebrospinal fluid, and it notes the new methodologies that can measure both endogenous and exogenous OT simultaneously, which thereby determine the source of measured OT in biological fluids. Next, this review highlights the utility of measuring urinary OT by summarizing the results of clearance rate studies in humans and marmosets, which characterize the timing that circulating OT enters urine and illustrate that endogenous releasers of OT also increase urinary OT. With the ability to reliably measure OT and AVP in urine and in blood, we can now study free-ranging captive, and non-captive primates to answer questions about the biology of social bonding that were not possible before. One procedural concern that this review also highlights is whether extraction of the peptides prior to assay is needed, as the values are higher in samples that have not been extracted. Studies indicate that extractions eliminate the interfering compounds that cause higher values. Across studies, to ensure the reliability of measuring OT for nonhuman primates, this review makes suggestions based on empirical evidence for how to correctly preserve samples and emphasizes the need to validate each assay for individual species.

Comparison of vitamin D metabolites in wild and captive baboons.

Vitamin D adequacy is essential for multiple physiologic processes. With limited exposure to sunlight for vitamin D3 synthesis, captive primates are supplemented with vitamin D3 (cholecalciferol). Vitamin D metabolite data from wild primates living indigenously could suggest optimum levels. The purpose of this study was to: 1) to explore whether baboons, a speciose genus whose members have significant exposed skin, coat color variation and wide geographical distribution, mirrors the skin pigmentation-vitamin D relationship found in humans; 2) compare vitamin D metabolite levels in wild and captive members of the same or similar baboon species; and 3) apply a recently developed method currently used in humans for measuring multiple vitamin D metabolites as a panel to explore if/how these metabolites can inform us on vitamin D sufficiency. Serum samples from males of three baboon species in the wild: Papio anubis (olive baboon, dark exposed skin), P. cynocephalus (yellow baboon, brown exposed skin), and P. hamadryas (hamadryas baboon, pink exposed skin), were compared with vitamin D supplemented captive olive baboons with sun exposure. Liquid chromatography/tandem mass spectrometry (LC/MS/MS) measured vitamin D and its main metabolites. Cholecalciferol, 25 hydroxyvitamin D2&3 (25(OH)D2&3 ), and 24,25 dihydroxyvitamin D2&3 (24,25(OH)2 D2&3 ), showed significant differences by species. The levels of cholecalciferol due to supplements in the captive olive baboons did not convert to higher 25(OH)D3 while the wild olive baboons exhibited the lowest levels for both cholecalciferol and 25(OH)D3 . Further metabolic conversion of 25(OH)D3 to 24,25(OH)2 D3 indicated that all baboons had more similar conversion ratios and these were within the same range found for humans that are depicted as having adequate vitamin D levels. This study provided evidence that exposed skin color does influence vitamin D3 levels, with lower levels in darker skinned species, but these differences are eliminated in the downstream metabolite conversion indicating strong regulatory control.

Neuroendocrine control in social relationships in non-human primates: Field based evidence.

Primates maintain a variety of social relationships and these can have fitness consequences. Research has established that different types of social relationships are unpinned by different or interacting hormonal systems, for example, the neuropeptide oxytocin influences social bonding, the steroid hormone testosterone influences dominance relationships, and paternal care is characterized by high oxytocin and low testosterone. Although the oxytocinergic system influences social bonding, it can support different types of social bonds in different species, whether pair bonds, parent-offspring bonds or friendships. It seems that selection processes shape social and mating systems and their interactions with neuroendocrine pathways. Within species, there are individual differences in the development of the neuroendocrine system: the social environment individuals are exposed to during ontogeny alters their neuroendocrine and socio-cognitive development, and later, their social interactions as adults. Within individuals, neuroendocrine systems can also have short-term effects, impacting on social interactions, such as those during hunting, intergroup encounters or food sharing, or the likelihood of cooperating, winning or losing. To understand these highly dynamic processes, extending research beyond animals in laboratory settings to wild animals living within their natural social and ecological setting may bring insights that are otherwise unreachable. Field endocrinology with neuropeptides is still emerging. We review the current status of this research, informed by laboratory studies, and identify questions particularly suited to future field studies. We focus on primate social relationships, specifically social bonds (mother-offspring, father-offspring, cooperative breeders, pair bonds and adult platonic friendships), dominance, cooperation and in-group/out-group relationships, and examine evidence with respect to the 'tend and defend' hypothesis.

Changes in physiological stress and behaviour in semi-free-ranging red-capped mangabeys (Cercocebus torquatus) following antiparasitic treatment.

Parasites are ubiquitous in wildlife populations, but physiological and behavioural responses of hosts to infection are difficult to measure. We experimentally treated semi-free-ranging red-capped mangabeys (Cercocebus torquatus) in Nigeria with antiparasitic drugs and examined subsequent changes in glucocorticoid production and individual behaviour. Because both parasites and stress impact energy balance and health, we measured (i) behavioural time re-allocation via activity budgets, (ii) social relationships (e.g. social connectivity and dominance hierarchy stability) and (iii) body condition. We collected triplicate faecal samples (n = 441) from 49 individuals prior to and following treatment. Cortisol levels fluctuated in parallel with parasite abundance. Elevations in cortisol, but not parasitism, were related to reduced body condition. Behaviour also shifted according to infection status, with uninfected individuals spending more time foraging and less time resting and vigilant compared with when they were infected. Time spent feeding, travelling or socializing did not differ between pre- and post-treatment time periods. Group cohesion, but not dominance stability, changed following treatment, suggesting parasite-induced social avoidance. Together, these findings show a coordinated response to infection that promotes host tolerance through stress and energy conservation, reduces transmission risk and increases protection when infected hosts are vulnerable.

Hormonal stimulation and paternal experience influence responsiveness to infant distress vocalizations by adult male common marmosets, Callithrix jacchus.

Parental experience and hormones play a large role in the common marmoset (Callithrix jacchus) father's care of their offspring. We tested the effect of exogenous estradiol or testosterone on the responsiveness of common marmosets to respond to infant distress vocalizations and whether males who haven't become fathers yet (paired males) would have increased responsiveness to infant distress calls with either steroid or whether parental experience is the most important component for the onset of paternal care. Sixteen male marmosets (8 fathers, 8 paired males) received a vehicle, low dose or high dose of estradiol and additional 16 males were tested with testosterone at three doses for their response either to a vocal control or a recording of an infant distress call for 10min. Without steroid stimulation fathers were significantly more likely to respond to the infant distress stimulus than paired males. Low dose estradiol stimulation resulted in a significant increase in fathers' behavioral response towards the infant distress stimulus but not in paired males. Fathers also showed a significant increase in infant responsiveness from the vehicle dose to the estradiol low dose treatment, but not to the estradiol high dose treatment. Testosterone treatment did not show significant differences between infant responsiveness at either dose and between fathers and paired males. We suggest that neither steroid is involved in the onset of paternal care behaviors in the marmoset but that estradiol may be involved in facilitating paternal motivation in experienced fathers.

Primate paternal care: Interactions between biology and social experience.

This article is part of a Special Issue "Parental Care".We review recent research on the roles of hormones and social experiences on the development of paternal care in humans and non-human primates. Generally, lower concentrations of testosterone and higher concentrations of oxytocin are associated with greater paternal responsiveness. Hormonal changes prior to the birth appear to be important in preparation for fatherhood and changes after the birth are related to how much time fathers spend with offspring and whether they provide effective care. Prolactin may facilitate approach and the initiation of infant care, and in some biparental non-human primates, it affects body mass regulation. Glucocorticoids may be involved in coordinating reproductive and parental behavior between mates. New research involving intranasal oxytocin and neuropeptide receptor polymorphisms may help us understand individual variation in paternal responsiveness. This area of research, integrating both biological factors and the role of early and adult experience, has the potential to suggest individually designed interventions that can strengthen relationships between fathers and their partners and offspring.

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus.

OBJECTIVE: Circannual variation in reproduction is pervasive in birds and mammals. In primates, breeding seasonality is variable, with seasonal birth peaks occurring even in year-round breeders. Environmental seasonality is reportedly an important contributor to the observed variation in reproductive seasonality. Given that food availability is the primary factor constraining female reproduction, predictions concerning responsiveness to environmental seasonality focus on females, with studies of males focusing primarily on social factors. We examined the influence of both environmental and social factors on male fecal testosterone (fT) and glucocorticoids (fGC) in moderately seasonally breeding white-faced capuchin monkeys (Cebus capucinus) in Costa Rica. METHODS: Over 17 months, we collected 993 fecal samples from 14 males in three groups. We used LMM to simultaneously examine the relative effects of photoperiod, fruit biomass, rainfall, temperature, female reproductive status (i.e., number of periovulatory periods, POPs), and male age and dominance rank on monthly fT and fGC levels. RESULTS: Male age and rank had large effects on fT and fGC. Additionally, some hormone variation was explained by environmental factors: photoperiod in the previous month (i.e., lagged photoperiod) was the best environmental predictor of monthly fT levels, whereas fGC levels were best explained by lagged photoperiod, fruit biomass, and rainfall. POPs predicted monthly fT and fGC, but this effect was reduced when all variables were considered simultaneously, possibly because lagged photoperiod and POP were highly correlated. CONCLUSIONS: Males may use photoperiod as a cue predicting circannual trends in the temporal distribution of fertile females, while also fine-tuning short-term hormone increases to the actual presence of ovulatory females, which may occur at any time during the year.

Measurement of 25-hydroxyvitamin D(2&3) and 1,25-dihydroxyvitamin D(2&3) by tandem mass spectrometry: A primate multispecies comparison.

Vitamin D metabolites are widely studied for their roles in bone health, immune functions, and other potential physiologic roles in humans. However, the optimal blood levels of vitamin D metabolites are still unclear. Various methods for measuring vitamin D metabolites have been used and recently liquid chromatography tandem mass spectroscopy (LC-MS/MS) has been adopted as the gold standard for vitamin D metabolite measurement. Here, we report the use of LC-MS/MS to measure 25-hydroxyvitamin D (25(OH)D(2&3)), and 1,25-dihydroxyvitamin D (1,25(OH)2D(2&3)), in three laboratory nonhuman primate species: common marmoset (Callithrix jacchus), rhesus macaque (Macaca mulatta), and cynomolgus macaque (Macaca fascicularis), and compare them to humans using the same technique. The nonhuman primates showed blood levels for 25(OH)D3 and 1,25(OH)2D3 significantly higher than human values with marmosets having the highest levels. Marmoset samples showed significantly more variability among individuals than those from macaques for both metabolites, but all three nonhuman primate species exhibited large variation within species for both 25(OH)D(2&3) and 1,25(OH)2D(2&3). Marmoset females had significantly lower values than the males for 25(OH)D3, while rhesus males showed a significant decrease in 25(OH)D3 with age. The most striking finding is the variation within species for vitamin D levels even in laboratory primates that have a controlled diet, UV exposure, and in some cases, genetic constraints. Similar variation in 25(OH)D responses to a fixed dose of oral vitamin D supplementation has been reported in humans. We suggest that these species can provide primate models for examining the factors influencing variation in the levels of vitamin D necessary for human and nonhuman primate health.

Neuroestradiol in the hypothalamus contributes to the regulation of gonadotropin releasing hormone release.

Release of gonadotropin releasing hormone (GnRH) from the medial basal hypothalamus (MBH)/median eminence region (S-ME) is essential for normal reproductive function. GnRH release is profoundly regulated by the negative and positive feedback effects of ovarian estradiol (E2). Here we report that neuroestradiol, released in the S-ME, also directly influences GnRH release in ovariectomized female monkeys, in which the ovarian source of E2 is removed. We found that (1) brief infusion of E2 benzoate (EB) to the S-ME rapidly stimulated release of GnRH and E2 in the S-ME of ovariectomized monkeys, (2) electrical stimulation of the MBH resulted in GnRH release as well as E2 release, and (3) direct infusion of an aromatase inhibitor to the S-ME suppressed spontaneous GnRH release as well as the EB-induced release of GnRH and E2. These findings reveal the importance of neuroestradiol as a neurotransmitter in regulation of GnRH release. How circulating ovarian E2 interacts with hypothalamic neuroestrogens in the control of GnRH release remains to be investigated.

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees.

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent-offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event--food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother-infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.

Hormones in infant rhesus monkeys' (Macaca mulatta) hair at birth provide a window into the fetal environment.

BACKGROUND: It is established that maternal parity can affect infant growth and risk for several disorders, but the prenatal endocrine milieu that contributes to these outcomes is still largely unknown. Recently, it has been shown that hormones deposited in hair can provide a retrospective reflection of hormone levels while the hair was growing. Taking advantage of this finding, our study utilized hair at birth to investigate if maternal parity affected fetal hormone exposure during late gestation. METHODS: Hair was collected from primiparous and multiparous mother and infant monkeys at birth and used to determine steroid hormones embedded in hair while the infant was in utero. A high-pressure liquid chromatography-triple quadrupole mass spectrometry technique was refined, which enabled the simultaneous measurement of eight hormones. RESULTS: Hormone concentrations were dramatically higher in neonatal compared to maternal hair, reflecting extended fetal exposure as the first hair was growing. Further, hair cortisone was higher in primiparous mothers and infants when compared to the multiparous dyads. CONCLUSION: This research demonstrates that infant hair can be used to track fetal hormone exposure and a panel of steroid hormones can be quantified from hair specimens. Given the utility in nonhuman primates, this approach can be translated to a clinical setting with human infants.