Andrew K. Birnie

Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata

The establishment and maintenance of stable, long-term male-female relationships, or pair-bonds, are marked by high levels of mutual attraction, selective preference for the partner, and high rates of sociosexual behavior. Central oxytocin (OT) affects social preference and partner-directed social behavior in rodents, but the role of this neuropeptide has yet to be studied in heterosexual primate relationships. The present study evaluated whether the OT system plays a role in the dynamics of social behavior and partner preference during the first 3 weeks of cohabitation in male and female marmosets, Callithrix penicillata. OT activity was stimulated by intranasal administration of OT, and inhibited by oral administration of a non-peptide OT-receptor antagonist (L-368,899; Merck). Social behavior throughout the pairing varied as a function of OT treatment. Compared to controls, marmosets initiated huddling with their social partner more often after OT treatments but reduced proximity and huddling after OT antagonist treatments. OT antagonist treatment also eliminated food sharing between partners. During the 24-h preference test, all marmosets interacted more with an opposite-sex stranger than with the partner. By the third-week preference test, marmosets interacted with the partner and stranger equally with the exception that intranasal-OT treatments facilitated initial partner-seeking behavior over initial contact with the stranger. Our findings demonstrate that pharmacological manipulations of OT activity alter partner-directed social behavior during pair interactions, suggesting that central OT may facilitate the process of pair-bond formation and social relationships in marmoset monkeys.

Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi)

Variation in the early postnatal social environment can have lasting effects on hypothalamic-pituitary-adrenal (HPA) axis stress responses. Both rats and macaque monkeys subjected to low quality or abusive maternal care during the early postnatal period have more pronounced HPA responses to environmental stressors throughout development and into adulthood compared to animals reared in higher quality early maternal environments. However, little is known about the relative contributions to HPA stress response styles in developing offspring in species in which offspring care is routinely provided by group members other than the mother, such as in cooperatively breeding mammals. Marmoset monkeys exhibit cooperative offspring rearing, with fathers and older siblings providing care in addition to that provided by the mother. We evaluated the effects of early maternal, paternal, and older sibling care on HPA responses to social separation across development in captive white-faced marmoset offspring (Callithrix geoffroyi). We monitored offspring care by mothers, fathers, and older siblings in marmosets for the first 60 days of life. Later in development, each marmoset experienced three standardized social separation/novelty exposure stressors at 6, 12, and 18 months of age. During separation, we collected urine samples and analyzed them via enzyme immunoassay for cortisol levels. Infants that received higher rates of rejections from the entire family group showed higher cortisol responses to social separation. This relationship was found when mothers, fathers, and older siblings, were analyzed separately as well. No differences in cortisol responses were found between offspring that received high and low rates of carrying or high and low rates of licking and grooming by any group member. In the cooperatively breeding marmoset, early social cues from multiple classes of caregivers may influence HPA stress responses throughout the lifespan.

Social isolation affects partner-directed social behavior and cortisol during pair formation in marmosets, Callithrix geoffroyi

Pair-bonded relationships form during periods of close spatial proximity and high sociosexual contact. Like other monogamous species, marmosets form new social pairs after emigration or ejection from their natal group resulting in periods of social isolation. Thus, pair formation often occurs following a period of social instability and a concomitant elevation in stress physiology. Research is needed to assess the effects that prolonged social isolation has on the behavioral and cortisol response to the formation of a new social pair. We examined the sociosexual behavior and cortisol during the first 90-days of cohabitation in male and female Geoffroys tufted-ear marmosets (Callithrix geoffroyi) paired either directly from their natal group (Natal-P) or after a prolonged period of social isolation (ISO-P). Social isolation prior to pairing seemed to influence cortisol levels, social contact, and grooming behavior; however, sexual behavior was not affected. Cortisol levels were transiently elevated in all paired marmosets compared to natal-housed marmosets. However, ISO-P marmosets had higher cortisol levels throughout the observed pairing period compared to Natal-P marmoset. This suggests that the social instability of pair formation may lead to a transient increase in hypothalamic-pituitary-adrenal (HPA) axis activity while isolation results in a prolonged HPA axis dysregulation. In addition, female social contact behavior was associated with higher cortisol levels at the onset of pairing; however, this was not observed in males. Thus, isolation-induced social contact with a new social partner may be enhanced by HPA axis activation, or a moderating factor.

Maternal androgen levels during pregnancy are associated with early-life growth in Geoffroy's marmosets, Callithrix geoffroyi

Fetal development is a critical period of physical development, and factors in the intrauterine environment can cause lasting effects on the growth and development of offspring. There is little research evaluating organizational effects of early androgen exposure of endogenous maternal origins on the prenatal and postnatal growth of offspring. We evaluated the association between maternal androgen levels during gestation and pre- and postnatal growth of offspring. Maternal androgen levels in marmoset females were measured using enzyme immunoassays of urine samples acquired during 18 pregnancies. Somatic measurements of the resulting 25 viable offspring were taken on postnatal days (PND) 2, 30, 60, 120, 180, 240, and 300. Maternal androgen levels during the first trimester were negatively associated with weight, body length, and several girth measurements (i.e., torso, head, chest, and arm circumference) of offspring on PND 2. First trimester maternal androgen was also negatively associated with physical growth during early and late infancy but seemed to be positively associated with a rebound in juvenile growth. Exposure to maternal androgen during early gestation led to both a reduction in birth weight and postnatal catch-up for both males and females, equally. Fetal growth retardation and the reprogramming of metabolic tissues by exposure to prenatal androgen could be mediating factors of suppressed postnatal growth.

The influence of androgenic steroid hormones on female aggression in 'atypical' mammals

Dimorphism on dominance and agonistic behaviour in mammals tends to be strongly biased toward males. In this review, we focus on a select few species of mammals in which females are as or more aggressive than males, and/or are dominant to males, and explore the role of androgenic hormones in mediating this important difference. While the data are not as clear-cut as those published on traditional laboratory mammals, our review highlights important endocrine substrates for both organizational and activational influences of steroids on female aggressive behaviour. We highlight areas in which further observations and experiments are crucial, especially the potential facilitative effects of androgens on female aggression. Finally, new and innovative techniques, including molecular genetics and receptor pharmacology, portend important insights into the ways in which androgenic hormones regulate aggressive behaviour in ‘atypical’ female mammals.

Gestational cortisol and social play shape development of marmosets' HPA functioning and behavioral responses to stressors

Both gestational cortisol exposure (GCE) and variability in postnatal environments can shape the later-life behavioral and endocrine outcomes of the hypothalamic-pituitary-adrenal (HPA) axis. We examined the influence of GCE and social play on HPA functioning in developing marmosets. Maternal urinary cortisol samples were collected across pregnancy to determine GCE for 28 marmoset offspring (19 litters). We administered a social separation stressor to offspring at 6, 12, and 18 months of age, during which we collected urinary cortisol samples and behavioral observations. Increased GCE was associated with increased basal cortisol levels and cortisol reactivity, but the strength of this relationship decreased across age. Increased social play was associated with decreased basal cortisol levels and a marginally greater reduction in cortisol reactivity as offspring aged, regardless of offspring GCE. Thus, GCE is associated with HPA functioning, but socially enriching postnatal environments can alter the effects associated with increased fetal exposure to glucocorticoids.

Prenatal Androgens Affect Development and Behavior in Primates

Maturation and differentiation persists throughout childhood, adolescence, and adult life into senescence; however, the foundation for normal postnatal development is established during fetal ontogeny. The organizational hypothesis proposes that nongenomic, environmental factors within the intrauterine environment attribute to prenatal programming (Phoenix et al. 1959). From the inception of this hypothesis over 50 years ago, researchers have documented the effects of exposure to prenatal steroid hormones, particularly androgens, on the behavior and growth of primate offspring. The effects of androgen within the intrauterine environment from maternal and exogenous sources can be observed in long-term changes to multiple developmental trajectories, including somatic growth, homeostatic functions of the body, and differentiation of sex-typical morphology, physiology, and behavior. Thus, the sensitivity and plasticity of the fetus during development toward androgens and other physiological cues from the mother and environment may underlie the development of diseases, a premise postulated by the Barker hypothesis (Barker 1998). In the current chapter, we discuss a number of prenatal and postnatal developmental outcomes associated with exposure to normal variations and excessive concentrations of androgens during prenatal life in human and nonhuman primates. In addition, it seems that the timing of androgen exposure during gestation and the sex of the fetus are two major factors that contribute to the concentration of androgens in the prenatal environment and the ultimate outcomes. Therefore, we also discuss the timing of androgen exposure during gestation and the sex of the fetus as modulating variables on the androgen-induced effects on development.

Behavioral characteristics of pair bonding in the black tufted-ear marmoset (Callithrix penicillata)

The present study describes how the development of a pair bond modifies social, sexual and aggressive behavior. Five heterosexual pairs of marmosets, previously unknown to each other, were formed at the beginning of the study. At the onset of pairing, social, sexual, exploratory and aggressive behaviors were recorded for 40 min. The animals were then observed for 20 min, both in the morning and afternoon for 21 days. The frequency and/or duration of behaviors recorded on Day 1 were compared to those recorded at later observations. The behavior displayed shortly after pairing should be completely unaffected by the pair bond, while such a bond should be present at later observations. Thus, it was possible to determine how the behavior between the pair was modified by the development of a pair bond. Social behaviors increased from Day 1 to Days 2-6 and all subsequent days observed. Conversely, other behaviors, such as open mouth displays (usually considered to be an invitation to sexual activity), had a high frequency during the early part of cohabitation but declined towards the end. Consequently, pair bonding manifests itself in an increased intensity of social behaviors. It is suggested that the intrinsically rewarding properties of grooming and perhaps other social behaviors turn the pair mate into a positive incentive, activating approach and further interactions when possible. Thus, the pair bond may be a motivational state activated by the conditioned incentive properties of the partner. This notion can explain all forms of pair bonds, including those occurring between individuals of the same sex and in promiscuous species.

Stress reactivity in young marmosets (Callithrix geoffroyi): Ontogeny, stability, and lack of concordance among co-twins

Variation in response styles in the hypothalamic-pituitary-adrenal (HPA) axis are known to be predictors of short- and long-term health outcomes. The nature of HPA responses to stressors changes with developmental stage, and some components of the stress response exhibit long-term individual consistency (i.e., are trait-like) while others are transient or variable (i.e., state-like). Here we evaluated the response of marmoset monkeys (Callithrix geoffroyi) to a standardized social stressor (social separation and exposure to a novel environment) at three different stages of development: juvenile, subadult, and young adult. We monitored levels of urinary cortisol (CORT), and derived multiple measures of HPA activity: Baseline CORT, CORT reactivity, CORT Area Under the Curve (AUC), and CORT regulation. Juvenile marmosets exhibited the most dramatic stress response, had higher AUCs, and tended to show poorer regulation. While baseline CORT and CORT regulation were not consistent within an individual across age, CORT reactivity and measures of AUC were highly correlated across time; i.e., individuals with high stress reactivity and AUC as juveniles also had high measures as subadults and adults, and vice-versa. Marmoset co-twins did not exhibit similar patterns of stress reactivity. These data suggest that regardless of the source of variation in stress response styles in marmosets, individually-distinctive patterns are established by six months of age, and persist for at least a year throughout different phases of marmoset life history.

Production and Perception of Sex Differences in Vocalizations of Wied’s Black-Tufted-Ear Marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wieds black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009.