Jeffrey A. French

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.

Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas

Within any hierarchical society, an individuals social rank can have profound effects on its health and reproductive success, and rank-related variation in these traits is often mediated by variation in endocrine function. Maternal effects mediated by prenatal hormone exposure are potentially important for non-genetic inheritance of phenotypic traits related to social rank, and thus for shaping individual variation in behaviour and social structure. Here we show that androgen concentrations in wild female spotted hyaenas (Crocuta crocuta) are higher during late gestation in dominant females than in subordinate females. Furthermore, both male and female cubs born to mothers with high concentrations of androgens in late pregnancy exhibit higher rates of aggression and mounting behaviour than cubs born to mothers with lower androgen concentrations. Both behaviours are strongly affected in other mammals by organizational effects of androgens, and both have important effects on fitness in hyaenas. Therefore, our results suggest that rank-related maternal effects of prenatal androgen exposure can adaptively influence offspring phenotype in mammals, as has previously been shown to occur in birds. They also suggest an organizational mechanism for the development of female dominance and aggressiveness in spotted hyaenas, traits that may offset the costs of extreme virilization.

Interactions among Paternal Behavior, Steroid Hormones, and Parental Experience in Male Marmosets (Callithrix kuhlii)

Male black tufted-ear marmosets (Callithrix kuhlii) contribute to the rearing of their offspring. Here we evaluated predictions of hypotheses suggesting that (1) T and E2 influence infant-care behavior in male marmosets, (2) levels of T and E2 are modulated by paternal experience, and (3) paternal behavior and levels of T and E2 in male marmosets covary with stress. We observed the behavior of marmosets in their family groups following the birth of infants and evaluated urinary concentrations of T, E2, and the stress hormone cortisol (CORT) among fathers before and after the birth of young. Urinary levels of T, E2, and CORT were lower among males who carried infants at high rates than males who carried at low rates, and T and CORT levels were negatively correlated with carrying rates across all males. Males had significantly lower T levels while carrying the second compared to the first litter and slightly lower rates of infant-carrying, possibly due to assistance provided by offspring of the first litter. There were increases in CORT levels of fathers after the birth of the first litter, but decreases in CORT after the birth of the second. Our results suggest a relationship in C. kuhlii between paternal behavior, hormones, and paternal experience. Rates of infant-carrying appear to be linked to hormone levels, and hormone levels in turn are affected by experience caring for young. Our data also suggest that T, E2, and CORT have synergistic influences on infant-carrying behavior or alternatively that associations between T and E2 and rates of infant-carrying are influenced by stress or other glucocorticoid-related variables. Finally, we propose a hypothesis suggesting that experience-related changes in hormones reinforce the commitment of males to successful breeding partnerships.

Psychosocial stress and urinary cortisol excretion in marmoset monkeys (Callithrix kuhli)

Activation of the hypothalamic-pituitary-adrenal (HPA) axis is one of the hallmarks of the physiological responses to psychosocial stressors. The most common method of assessing HPA function is via the measurement of plasma cortisol levels. However, venipuncture involves capture and restraint, which can modify HPA function. We validated a noninvasive procedure for monitoring HPA responses to stressors by measuring excretion of free urinary cortisol. Samples collected throughout the day displayed marked circadian variation, with low cortisol values in first-void samples, followed by a mid-morning peak in cortisol excretion. Concentrations of excreted cortisol declined throughout the day. Exposing marmosets to mild and moderate stressors (11 h isolation in a small cage and manual restraint) increased excreted cortisol concentrations in a dose-dependent fashion: isolation in a small cage led to elevated cortisol in afternoon samples, while manual restraint and isolation produced elevated cortisol in both morning and afternoon samples. The marmoset HPA is differentially sensitive to rather subtle variations in stressors, and these results show that urinary cortisol excretion is a valid and sensitive index of the HPA response to these stressors.

Close Proximity of the Heterosexual Partner Reduces the Physiological and Behavioral Consequences of Novel-Cage Housing in Black Tufted-Ear Marmosets (Callithrix kuhli)

The present studies assessed the extent to which heterosexual pairmates could buffer marmosets (Wieds black tufted-ear marmoset, Callithrix kuhli) against stress. Six male and six female marmosets from established groups were exposed to two experimental manipulations together with a control condition. Each condition lasted a total of 4 days. For the two experimental conditions, animals were removed from the family group and housed in a novel cage for 48 h in either the presence or the absence of the heterosexual pairmate. During the 48-h novel-cage housing period and for 48 h upon reunion of the subjects with the family group, concentrations of urinary cortisol were measured in the first void sample of the day and behavioral observations were conducted. When animals were housed alone in a novel cage they exhibited significant elevations in levels of urinary cortisol after 24 and 48 h of novel-cage exposure. In contrast, when marmosets were housed in the novel cage in the presence of the pairmate, levels of urinary cortisol did not change across the 4-day period. The presence of the social partner also reduced the behavioral manifestations of exposure to novelty. Upon reunion with the family group, animals that had been housed in the novel cage alone spent significantly more time in close proximity to the pairmate than animals that had been housed with the partner. A second experiment was conducted to determine the effect that separation from the pairmate, only (independent of any effects of novelty), had on levels of cortisol. Concentrations of urinary cortisol were measured in subjects housed in the familiar home cage, but in the absence of the pairmate, over a 48-h period and compared to concentrations of excreted cortisol immediately prior to separation. Separation from the pairmate did not elevate cortisol levels when the subject was housed in the home cage, suggesting that elevated cortisol levels in animals housed alone in the novel cage were in response to novelty exposure rather than to separation from the pairmate. Since the physical presence of the heterosexual partner reduced the physiological and behavioral effects of novel-cage housing, social attachments might function as homeostatic regulators of HPA function in marmosets.

Fetal testosterone surge: Specific modulations induced in male rats by maternal stress and/or alcohol consumption

Plasma testosterone (T) was measured in control male and female rats on gestational days 16, 17, 18, 19, and 20 and on days 17-20 in males from dams who were fed ethanol and/or were stressed during pregnancy. Circulating T in control males showed an earlier rise, yielding a longer period of prenatal T elevation, than was reported previously (Endocrinology 106 (1980)306). Compared to control males, exposure to alcohol-alone augmented T on days 18 and 19, stress-alone attenuated prenatal T, and the combination of stress and alcohol completely blocked the normal rise in T between days 17 and 18. When these prenatal alterations in T are viewed along with effects these same treatments have on the postparturient T surge (Horm. Behav. 41 (2002) 229), a possible explanatory mechanism emerges for the uniquely different behavioral patterns of sexual behavior differentiation induced in males by prenatal exposure to alcohol, stress, or both factors. Whereas the potential for feminine behavior is retained to the extent that either the prenatal or the neonatal T surge is attenuated, the male potential is more sensitive to reductions in the fetal surge and is maximally disrupted if both the prenatal and the postparturitional T surges are suppressed.

Social and reproductive conditions modulate urinary cortisol excretion in black tufted‐ear marmosets (Callithrix kuhli)

The links between psychosocial stress, social status, reproductive function, and urinary cortisol were assessed in social groups of black tufted‐ear marmosets (Callithrix kuhli). Urinary cortisol excretion was monitored in cases of intrafamily conflict (“sibling fights”) and in daughters in four distinct social contexts: in the family group, while housed singly or in same‐sex pairs, and while paired with a male pairmate. Cortisol excretion was elevated in participants in intra‐family conflict on the day of and the day following the conflict, relative to concentrations a week prior to or following the conflict. Daughters in natal family groups had concentrations of cortisol that did not differ from reproductively active adult females. This finding held for daughters who were either anovulatory or undergoing ovulatory cycles while in the natal family group. Natal family members and male pairmates exerted buffering effects on levels of activity in the hypothalamic pituitary adrenal axis (HPA) in female C. kuhli. Placing females in solitary housing led to significantly increased cortisol excretion. In the 2 months subsequent to pairing with a male partner, excreted cortisol concentrations in females declined significantly. Daughters removed from their natal family group and housed with a sister did not exhibit increased cortisol levels. These data reveal that activity in the (HPA) axis in marmosets is sensitive to psychosocial stressors, and that urinary cortisol can provide a useful quantitative measure of HPA reactivity. As in other callitrichids, delayed breeding in daughters and reproductive anomalies in C. kuhli appear to be mediated by mechanisms other than elevated HPA activity. Am. J. Primatol. 42:253–267, 1997.

Urinary steroid and gonadotropin excretion across the reproductive cycle in female Wied's black tufted-ear marmosets (Callithrix kuhli)

Details of the endocrinology of reproduction in the genus Callithrix are known only for the common marmoset, C. jacchus. This paper presents the patterns of urinary pregnandiol‐3‐glucuronide (PdG), urinary estrone conjugates (E1C), and gonadotropin excretion throughout the reproductive cycle of Wieds black tufted‐ear marmoset (C. kuhli) as determined via steroid conjugate enzyme immunoassays (EIA) and gonadotropin radioimmunoassays (RIA). Postpartum ovulation occurred at 13.6 ± 1.2 days after parturition (n = 12) and was characterized by low PdG and E1C concentrations accompanied by a spike in luteinizing hormone (LH)/chorionic gonadotropin (CG) concentration. After conception, PdG concentrations increased dramatically until they dropped to periovulatory concentrations in the third trimester of pregnancy. Mean PdG concentrations in the first and second trimesters (33.7 ± 8.4 and 39.0 ± 10.9 μg/mg creatinine, respectively) were three times that of third trimester concentrations (11.7 ± 1.4 μg/mg Cr; n = 8). Urinary concentrations of E1C rose more gradually during pregnancy and remained higher prepartum than urinary concentrations of PdG. Urinary gonadotropin concentrations also increased after conception (first trimester concentrations = 24.5 ± 4.5 ng/mg Cr) and continued to increase in the second trimester (51.4 ± 7.6 ng/mg Cr), until they finally decreased in the third trimester (mean = 7.9 ± 1.4 ng/mg Cr; n = 8). The interbirth interval was 156.3 ± 2.9 days (n = 6), with a gestation of 143.1 ± 1.6 days (n = 8). Nonconceptive cycle length was 24.9 ± 0.6 days (n = 4). The results of this study suggest strong similarities in reproductive parameters in the genus Callithrix.

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.

The Effect of Resistive Exercise Rest Interval on Hormonal Response, Strength and Hypertrophy with Training

Buresh, R, Berg, K, and French, J. The effect of resistive exercise rest interval on hormonal response, strength, and hypertrophy with training. J Strength Cond Res 23(1): 62-71, 2009- The purpose of this study was to compare the effects of different between-set rest periods (1 and 2.5 minutes) on changes in hormone response, strength, arm cross-sectional area (CSA), thigh muscular cross-sectional area (MCSA), and body composition during a 10-week training period. Twelve untrained males (24.8 ± 5.9 years) engaged in resistance training using either 1 minute (short rest [SR], n = 6) or 2.5 minutes (long rest [LR], n = 6) of rest between sets, with a load that elicited failure on the third set of each exercise. Body composition, thigh MCSA, arm CSA, and five-repetition maximum (RM) squat and bench press were assessed before and after training. Blood samples were collected after exercise in weeks 1, 5, and 10. In week 1, postexercise plasma testosterone levels were greater in SR (0.41 ± 0.17 mmol·L−1) than in LR (0.24 ± 0.06 mmol·L−1, p < 0.05), and postexercise cortisol levels were greater in SR (963 ± 313 mmol·L−1) than in LR (629 ± 127 mmol·L−1, p < 0.05). Week 1 postexercise GH levels were not different (p = 0.28). The differences between hormone levels in weeks 5 and 10 were not significant. Arm CSA increased more with LR (12.3 ± 7.2%) than with SR (5.1 ± 2.9%, p < 0.05). There were no differences in strength increases. These results show that in healthy, recently untrained males, strength training with 1 minute of rest between sets elicits a greater hormonal response than 2.5-minute rest intervals in the first week of training, but these differences diminish by week 5 and disappear by week 10 of training. Furthermore, the hormonal response is highly variable and may not necessarily be predictive of strength and lean tissue gains in a 10-week training program.