Changes in prolactin and glucocorticoid levels in cotton-top tamarin fathers during their mate's pregnancy: the effect of infants and paternal experience

We have previously shown that paternally experienced cotton-top tamarin fathers (Saguinus oedipus) had significant increases in prolactin and glucocorticoids at the midpoint of their mate's pregnancy, whereas less experienced fathers showed prolactin increases only the month before offspring birth [Ziegler & Snowdon, Hormones & Behavior 38:159-167, 2000; Ziegler et al., Hormones & Behavior 45:84-92, 2004]. These results could be owing to differing paternal experience or from paternal care given to previous offspring. To test the relative role of infant cues and paternal experience in these hormonal changes, we paired four paternally experienced tamarin fathers with a novel, primiparous female and monitored hormone levels during their first pregnancy together. No fathers showed the significant mid-pregnancy increase in prolactin seen previously. However, all fathers showed increases in cortisol and significant peaks of corticosterone in mid-pregnancy. The increase in corticosterone was consistent with previous data occurring in each male during the same week or the week following the urinary cortisol increase shown by his mate. These data may suggest that the elevated mid-gestation prolactin seen previously in experienced males may be owing to the presence of offspring from the previous set of infants. In contrast, increased cortisol and corticosterone occurred independently of infant cues and may be related to previous paternal experience. We therefore conclude that both offspring presence and paternal experience contribute to the hormonal changes seen in experienced cotton-top tamarin fathers during their mate's pregnancy.     

Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus)

Callithrix jacchus infants are raised in complex family environments where most members participate in rearing the young. Many studies examining male parental behavior have focused on the carrying of infants with observations made within the family context. However, interference from family members can make it difficult to assess the father's motivation to care for infants. Our goals were to develop a testing paradigm for determining an individual's response to infant stimuli separate from family influences, compare a male's motivation to respond to an infant stimulus outside the family with his paternal behavior within the family, to compare responses to infant stimuli of parentally experienced versus inexperienced males and finally to develop a reproducible and standardized method of testing male responsiveness to infant stimulus that could serve to evaluate hormonal manipulations. Fifteen experienced common marmoset fathers were evaluated using three different measures of parental behavior: (1) instantaneous scan sampling, (2) continuous focal sampling in the family, and (3) continuous focal sampling of males presented with four infant stimuli: familiar and unfamiliar infants, familiar and unfamiliar infant vocalizations. Six parentally inexperienced males (non-fathers) served as controls. Males that carried the most in the family were typically the same males that responded most to the infant vocalization tests. Experienced fathers did not differ in their latency to enter the stimulus cage for any of the four infant stimuli response tests while inexperienced males took significantly longer to enter the stimulus cage. In addition, fathers expressed a greater frequency of infant-directed behavior than did the inexperienced males during the unfamiliar infant and unfamiliar vocalization tests. These studies show that experienced male marmosets are highly motivated to interact with infant stimuli and that there is interindividual variability in response to infant vocalizations. Testing males outside of the family allows for a clear assessment of male's interest in infant stimuli in both parentally experienced fathers and inexperienced males.     

Exposure to infant scent lowers serum testosterone in father common marmosets (Callithrix jacchus)

Common marmoset (Callithrix jacchus) males are bi-parental non-human primates that show extensive paternal behaviour. Fathers are in direct sensory contact with their infants during the natal period. We found that fathers exposed to isolated scents of their infant displayed a significant drop in serum testosterone levels within 20min after exposure, whereas parentally naive males did not. These data suggest that infant's scent may have a causal role in regulating paternal testosterone in their fathers. This is the first study to demonstrate that olfactory cues have an acute effect on paternal care.     

Testosterone responses to competition in men are related to facial masculinity

Relationships between androgens and the size of sexually dimorphic male traits have been demonstrated in several non-human species. It is often assumed that a similar relationship exists for human male faces, but clear evidence of an association between circulating testosterone levels and the size of masculine facial traits in adulthood is absent. Here we demonstrate that, after experimentally determined success in a competitive task, men with more a masculine facial structure show higher levels of circulating testosterone than men with less masculine faces. In participants randomly allocated to a 'winning' condition, testosterone was elevated relative to pre-task levels at 5 and 20 min post-task. In a control group of participants allocated to a 'losing' condition there were no significant differences between pre- and post-task testosterone. An index of facial masculinity based on the measurement of sexually dimorphic facial traits was not associated with pre-task (baseline) testosterone levels, but was associated with testosterone levels 5 and 20 min after success in the competitive task. These findings indicate that a man's facial structure may afford important information about the functioning of his endocrine system.     

Salivary hormone concentrations in mothers and fathers becoming parents are not correlated

A time- and date-matched set of saliva samples (N = 229) from nine couples first expecting, and then caring for, their first child were used to test whether hormone changes in the father could be predicted by the hormonal status of the mother. Testosterone, cortisol, and estradiol were quantified from saliva. Neither testosterone nor estradiol concentration was correlated within couples before or after the birth, although there was a positive correlation for cortisol concentration in the mother and father before the birth. As the hormone that might be influenced by chemical signals, that already played a similar role in men and women, and that had been empirically linked to paternal behavior, cortisol concentration was also compared with sex steroid concentrations. The mother's cortisol concentration was positively correlated to the father's testosterone concentration, and the mother's testosterone concentration was positively correlated with the father's cortisol concentration. However, both effects were similar in magnitude to the cortisol to cortisol correlation, and all could parsimoniously be explained by similar responses to a shared environment. Thus, this analysis rejects parallels in peripheral hormone concentrations of estradiol, testosterone, and cortisol in mothers and fathers. However, the available data were not able to test or reject hypotheses about local neuroendocrine homology, nor to control for masking effects of other hormonal demands on men and women, nor to determine the relative importance of shared environment versus mother-father signaling.     

Testosterone levels and their associations with lifetime number of opposite sex partners and remarriage in a large sample of American elderly men and women

Testosterone (T) has been argued to modulate mating and parenting behavior in many species, including humans. The role of T for these behaviors has been framed as the challenge hypothesis. Following this hypothesis, T should be positively associated with the number of opposite sex partners a male has. Indeed research in humans has shown that T is positively related to the number of opposite sex partners a young man has had. Here we test, in both men and women, whether this relationship extends to the lifetime number of sex partners. We also explored whether or not T was associated with current marital status, partnership status and whether or not the participant remarried. Using a large sample of elderly men and women (each sample n > 700), we show that T is positively and sizably associated with the number of opposite sex partners in men. When controlling for potential confounding variables such as educational attainment, age, BMI, ethnicity, specific use of a medication and time of sampling this effect remained. For women, the relationship between T and number of opposite sex partners was positive but did not prove to be robust. In both men and women there was no evidence for an association between T and current marital status and partnership status (being in a relationship or not). However, remarriage was positively associated with T, but only in males. Results are discussed with reference to the literature on T and sex partners, remarriage and more broadly the challenge hypothesis.     

Effects of motherhood on physiological and subjective responses to infant cries in teenage mothers: a comparison with non-mothers and adult mothers

The present study was designed to determine whether becoming a mother during the adolescent period changes maternal responsiveness or maternal motivation, assessed through hormonal, autonomic, and hedonic responses to recorded infant cries and interactions with their babies. Fifty-six teen mothers were compared to 58 teen non-mothers and 49 adult mothers. Teen mothers reported more sympathy and alertness in response to recorded infant cries compared to non -mother teens; however, among the teen women there were no differences between mothers and non-mothers in heart rate and cortisol responses to infant cries. In contrast, in comparison to adult mothers, teen mothers reported the same levels of sympathy and alertness to infant cries; however, adult mothers showed an 'alerted' pattern of heart rate and cortisol response to infant cries not seen in the teen mother group. Inclusion of the covariate, fathers' employment classification as an index of SES or time of testing and cortisol sampling did not affect this pattern of results. Taken together, these results show that where self-report is used as a measure of maternal responsiveness, teen mothers are no different in responsiveness than adult mothers; however, where physiological and interactional measures of responsiveness are considered, teen mothers are less likely to show heightened or selective responses to infant cries or respond 'attentively' to the infant.     

Hormonal and experiential predictors of infant survivorship and maternal behavior in a monogamous primate (Callicebus cupreus)

To better understand the roles that hormones and experience play in infant survival and maternal behavior in a biparental primate species, we analyzed urinary estrone (E(1)C) and pregnanediol glucuronide (PdG) from 24 socially housed titi monkey (Callicebus cupreus) females over 54 pregnancies (N = 1,430 samples). Pregnancies were categorized according to whether the infant survived (N = 35) or not (N = 19), and by maternal parity (primiparous: N = 9; multiparous: N = 45). Mothers of infants that survived had a significantly greater drop in PdG from the third trimester to the first week postpartum than mothers of infants that did not survive. Multiparous mothers had a greater increase in PdG from the first to the third trimester as well as greater increases in the E(1)C:PdG ratio from the first to the third trimester and from the third trimester to the first week postpartum. There were positive relationships between third trimester PdG and maternal carrying and nursing during the first week postpartum, and between maternal age and carrying during the infant's first month of life. There was a negative correlation between maternal age and PdG during the third trimester. These results suggest that elevated progesterone during late pregnancy followed by progesterone withdrawal immediately following parturition is associated with greater probability of infant survivorship and maternal behavior in this species, and that older females engage in more postpartum maternal care.     

Testosterone and prolactin in two songbirds that differ in paternal care: the Blue-headed Vireo and the Red-eyed Vireo

We investigated the hypothesis that species differences in paternal care in birds may result from differences in concentrations of circulating testosterone (T) and prolactin (PRL). Concentrations of plasma T and PRL were compared in breeding Blue-headed Vireos (Vireo solitarius) and Red-eyed Vireos (Vireo olivaceus), passerine congeners with biparental and maternal incubation, respectively. In male Blue-headed Vireos, plasma T remained low from prenesting to fledgling stages; whereas in male Red-eyed Vireos, plasma T was highest during prenesting and progressively decreased during incubation, nestling, and fledgling stages. In male Blue-headed Vireos, plasma PRL was similar to that in female Blue-headed Vireos and was higher than in male Red-eyed Vireos at all breeding stages. Plasma PRL increased in male Red-eyed Vireos at the incubation stage and remained moderately elevated through the nestling and fledgling stages. In male Blue-headed Vireos, the combination of high PRL and low T during the prenesting stage may promote brood patch formation and nest building, and, at later stages, incubation and feeding of young. In male Red-eyed Vireos, high PRL and low T during incubation and nestling stages may facilitate the feeding of young, as seen in males of other species. Our observations support the hypothesis that differences in paternal care reflect differences in circulating T and PRL.     

Prenatal household size and composition are associated with infant fecal bacterial diversity in Cebu,Philippines

Objectives

The gut microbiome (GM) connects physical and social environments to infant health. Since the infant GM affects immune system development, there is interest in understanding how infants acquire microbes from mothers and other household members.

Materials and Methods

As a part of the Cebu Longitudinal Health and Nutrition Survey (CLHNS), we paired fecal samples (proxy for the GM) collected from infants living in Metro Cebu, Philippines at 2 weeks (N = 39) and 6 months (N = 36) with maternal interviews about prenatal household composition. We hypothesized that relationships between prenatal household size and composition and infant GM bacterial diversity (as measured in fecal samples) would vary by infant age, as well as by household member age and sex. We also hypothesized that infant GM bacterial abundances would differ by prenatal household size and composition.

Results

Data from 16 S rRNA bacterial gene sequencing show that prenatal household size was the most precise estimator of infant GM bacterial diversity, and that the direction of the association between this variable and infant GM bacterial diversity changed between the two time points. The abundances of bacterial families in the infant GM varied by prenatal household variables.

Conclusions

Results highlight the contributions of various household sources to the bacterial diversity of the infant GM, and suggest that prenatal household size is a useful measure for estimating infant GM bacterial diversity in this cohort. Future research should measure the effect of specific sources of household bacterial exposures, including social interactions with caregivers, on the infant GM.

     

Behavioral changes associated with introductions of male maned wolves (Chrysocyon brachyurus) to females with pups

Three male maned wolves were successfully introduced to their mates and 7‐ to 12‐week‐old pups at the Houston Zoological Gardens and Fossil Rim Wildlife Center in 1994 and 1995. The introductions took 3–7 weeks and had three stages: 1) allowing the male to see the female and pups through a chain‐link panel or a full chain‐link fence, 2) introducing the male and female without the pups present, and 3) introducing the male to the pups. For 7 days before Stage 2 and 7 days during Stage 3, the adults were observed for 150 hr. The amount of time they spent active and the amount of time they spent near the pups were recorded, as well as all behaviors they directed to the pups. After the males were introduced, the females' activity decreased, and the males' activity increased. The females spent less time near the pups after the introduction. The introduction did not affect the females' rates of affiliative or aggressive behaviors to the pups, and there was no difference between males' and females' rates of affiliative or aggressive behaviors. This introduction procedure offers an alternative to leaving the male with the pups from the time they are born. The adults' behavioral changes after the introduction show the benefits that occur when captive male maned wolves are allowed to help rear their pups. Zoo Biol 18:189–197, 1999. © 1999 Wiley‐Liss, Inc.     

Monthly patterns of testosterone and behavior in prospective fathers

The individual time patterns of salivary testosterone of adult healthy men, self-reported sexual behavior and their co-occurrence with regular weekly or monthly intervals were studied. Twenty-seven volunteer males (mean age 33 +/- 1 years) collected daily morning saliva over a period of 90 days. Evening questionnaires provided daily information on sexual activity. From the saliva, testosterone immunoreactive substances were determined using enzyme immunoassay. To detect events in which increases of testosterone were associated with sexual activity and at the same time controlling for regular internal patterns in men, data were analyzed using Theme software. First results indicated a varying number of complex nonrandom interaction patterns of testosterone with sexual activity, but also with weekly (i.e., Saturdays) and monthly intervals (i.e., 28-day full-moon intervals). The social context of the occurrence of specific pattern combinations was elaborated using parameters from the men's self-reported general life history profiles. Peak hormone levels occurred around weekends in the majority of the males. The 28-day monthly interval coincided with testosterone peaks only in those of the paired men who reported a current wish for children ("prospective fathers"), but not in unpaired men or in those who did not wish to have children with their current partner. Rather than representing a direct regular pattern of the male testosterone per se, the observed patterns suggest that men have the facultative potential to adjust their testosterone responses to their female partner's cycle. In line with the interactions between behavior and androgens observed in vertebrates in general, this study adds an example of the mutual character of hormone-behavior interactions and, thus, for the social context of testosterone patterns in human males.     

Altered Luteinizing Hormone and Testosterone Secretion in Middle‐Aged Obese Men with Obstructive Sleep Apnea

Objective: To elucidate the causes for the decline in testosterone levels observed in men with obstructive sleep apnea (OSA). Research Methods and Procedures: We determined serum luteinizing hormone (LH) and testosterone levels every 20 minutes between 7 pm and 7 am with simultaneous sleep recordings in five obese middle‐aged men with OSA, in five age‐ and BMI‐matched controls, and in six lean young healthy men. Results: The mean and area under the curve (AUC) values of LH and testosterone were significantly lower in men with OSA compared with controls. Young controls had significantly more testosterone pulses of shorter interpulse duration than OSA subjects and middle‐aged controls. After adjusting for age and BMI, the three groups differed in mean and AUC values of LH and testosterone. Analysis of covariance, using BMI as a covariate, revealed a statistically significant group effect on mean and AUC testosterone values (p = 0.03; p < 0.003, respectively). Eliminating young controls, there was a significant positive correlation between the amount of LH and testosterone secreted at night. After partialling out age alone and BMI alone, the mean LH and mean testosterone were still positively correlated. Discussion: Thus, OSA is associated with decreased pituitary‐gonadal function. The decline in testosterone concentrations is due to obesity and advanced age and to a lesser degree to sleep fragmentation and hypoxia.     

Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse

Maternal behaviour has profound, long-lasting implications for the health andwell-being of developing offspring. In the monogamous California mouse(Peromyscus californicus), care by both parents is critical foroffspring survival. We tested the hypothesis that similar to maternal care inrodents, paternal huddling and grooming (HG) behaviour can be transmitted to futuregenerations via behavioural mechanisms. In California mice, testosterone maintainspaternal HG behaviour. In the present study, we randomly assigned a group of maleCalifornia mice to castration or sham-operated conditions and allowed them to raisetheir offspring normally. Adult sons of these males were paired with a female, andthey were observed interacting with their own offspring. We found that like theirfathers, the sons of castrated males huddled and groomed their young at lower levelsthan the sons of sham-operated fathers. The sons of castrates also retrieved pupsmore frequently. When both parents were present, the sons of castrates also showed atrend towards engaging in less exploratory behaviour. These data support thehypothesis that paternal behaviour, like maternal behaviour, can be transferred tofuture generations via epigenetic mechanisms and suggest that in a biparental speciesboth parents contribute to offspring behavioural development.     

Seasonal levels of LH, FSH, testosterone and prolactin in adult male pudu (Pudu puda)

Seasonal levels of LH, FSH, testosterone (T) and prolactin (PRL) were determined in plasma of six captive adult male pudu (Pudu puda) kept in Concepcion, Chile. Average PRL levels exhibited one peak (28 ng/ml) in December (summer); minimal levels (3 to 6 ng/ml) were detected between April and July. FSH concentrations remained at peak levels (54–63 ng/ml) from December until March; minimal values (25–33 ng/ml) were detected from April until October. T levels exhibited two, almost equal peaks; the first peak (2.8 ng/ml) was detected in March (rut) and the second one (2.7 ng/ml) in October (spring). Both T peaks were preceded by an earlier elevation of LH in February and July (both around 1.3 ng/ml). During the fall, only the alpha male exhibited a sharp peak of T (8.4 ng/ml), whereas in the spring five out of six bucks demonstrated an increase of T levels. Two peaks of LH and T and the 4 months of elevated FSH may be related to a long period of spermatogenesis observed in this species.     

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.     

The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care.     

Testosterone is positively associated with risk taking in the Iowa Gambling Task

The association between testosterone and economic risk is not well-understood and is understudied. The present study aimed to further characterize what if any relationship testosterone has with risky economic decisions. To do so, 154 participants (78 men) completed the Iowa Gambling Task (IGT) (Bechara et al., 1994) and also provided saliva samples, which were assayed for endogenous testosterone levels using radioimmunoassay. High-levels of endogenous testosterone were associated with choosing less frequently from advantageous IGT decks of cards, indicating greater risk taking. The data showed that the effects of testosterone on IGT performance were similar for men and women. High-testosterone women and high-testosterone men made riskier choices than their low-testosterone counterparts of the same sex, and this effect was pronounced in women. Thus, high levels of testosterone are associated with willingness to incur greater risk in both sexes.