Prolactin, fatherhood, and reproductive behavior in human males

Although humans are considered unusual among mammals for the intensity of care that fathers often provide offspring, little is known about the hormonal architecture regulating human paternal investment. Prolactin has important reproductive functions in both female and male mammals and other taxa, making it a candidate regulator of human paternal behavior. Notably, prolactin is higher during periods of offspring care in some species, but it is unknown if this pattern occurs in human fathers. We draw on a sample of men (n = 289; age 21-23 at baseline) from Metropolitan Cebu City, Philippines to evaluate relationships between prolactin, assayed from dried blood spots, and components of reproductive behavior and relationship status. In this sample, fathers had higher prolactin than nonfathers (P = 0.006), and fathers of infants had borderline higher prolactin than fathers of older children (P = 0.054). Among single nonfathers at baseline (2005), baseline prolactin did not predict who transitioned to fatherhood by follow-up 4.5 years later. Among nonfathers, men with greater prolactin reported more lifetime sexual partners (P = 0.050) as well as more sexual activity in the month before sampling (P = 0.060). Our results suggest that fathers in Cebu have higher prolactin than nonfathers, with hormone levels highest among fathers of young infants. Although these findings are generally consistent with evidence from other species for pronurturing effects of prolactin, evidence for positive relationships between the hormone and measures of sexual behavior at Cebu point to likely complexities in the hormone's involvement in male reproductive strategy.     

Hormonal changes in mammalian fathers

Known and hypothesized relationships between steroid (estradiol, testosterone, and cortisol) and peptide (oxytocin, vasopressin, and prolactin) hormones and the expression of mammalian paternal behavior are reviewed. Emphasis is placed on newly emerging animal models, including nonhuman primates and men, with elaborate paternal behavior repertoires. Currently available data are broadly consistent with a working hypothesis that the expression of parental behavior will involve homologous neuroendocrine circuits in male and females. Understanding the neuroendocrinology of paternal behavior is an emerging research opportunity in behavioral neuroscience.     

The effects of social context on the hormonal and behavioral responsiveness of human fathers

We tested first-time fathers with their 22-month old toddlers to determine whether social context variables such as pre-test absence from the child and presence of the mother affected physiological measures associated with paternal responsiveness. Heart rate and blood pressure readings as well as blood samples to determine prolactin, testosterone and cortisol levels were taken before and after the 30-min father–toddler interactions. Fathers were tested on a day when they were away from their child for several hours before testing (‘without-child’ day) and on another day where they remained with their child throughout the day (‘with-child’ day). Most measures decreased over the 30-min test period but relative decreases were context-dependent. Men maintained higher prolactin levels when they were away from their children longer before testing on the ‘without-child’ day. Cortisol levels decreased during both tests and they decreased more on the ‘with-child’ day for men who had spent more time alone with their toddler before the test. Heart-rate and diastolic (but not systolic) blood pressure decreased more on the ‘with-child’ day than on the ‘without-child’ day. Fathers' testosterone levels decreased when their partners were less involved in the interactions. Compared to men with high responsiveness ratings on both days, men whose responsiveness increased after being away from their child on the ‘without-child’ day maintained higher systolic blood pressure and had a greater decrease in testosterone levels. We conclude that context may be more important in determining fathers' physiological responses to child contact than has previously been appreciated, particularly for some individuals.     

Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population

Recent evidence suggests that, in humans, variations in testosterone (T) levels between men reflect their differential allocation in mating versus parenting efforts. However, most studies have been conducted in urbanized, monogamous populations, making generalizations from them questionable. This study addresses the question of whether indicators of male reproductive effort are associated with variations in salivary T levels in a polygynous population of agriculturists in rural Senegal. We first show that pair-bonding and/or transition to fatherhood is associated with T profiles: married fathers (N = 53) have lower morning and afternoon T levels than unmarried non-fathers (N = 28). Second, among fathers, individual differences in parenting effort, as well as variations in mating effort, predict morning T levels. Indeed, men highly investing in parental care show lower morning T levels. Moreover, among men under 50, polygynous men show higher morning T levels than monogamous men. Taken together with previous results in monogamous settings, these findings suggest that the endocrine regulation of reproductive effort is probably a general feature of human populations.     

Testosterone and prolactin are associated with emotional responses to infant cries in new fathers

To determine the responsiveness of new fathers and non-fathers toward infant cues, we exposed fathers and non-fathers to infant cries and to control stimuli and we measured affective, heart-rate, and endocrine responses, including salivary testosterone and cortisol and plasma prolactin concentrations prior to and after cry presentations. We found that (1) fathers hearing the cry stimuli felt more sympathetic and more alert compared to groups who did not hear the cries or to non-fathers who heard the cries; (2) fathers and non-fathers with lower testosterone levels had higher sympathy and/or need to respond to the infant cries than fathers with higher testosterone levels; (3) fathers with higher, as opposed to lower, prolactin levels were also more alert and more positive in response to the cries; (4) fathers hearing the cry stimuli showed greater percentage increase in testosterone than fathers not hearing the cry stimuli; (5) experienced fathers hearing the cries showed a greater percentage increase in prolactin levels compared to first-time fathers or to any group of fathers hearing control stimuli; finally, (6) partial correlations with parity and experience entered as a covariates indicated that both experience and testosterone contributed to the variance in fathers' affective responses to infant cries. Taken together, these results indicate that, as with a number of other biparental species, human fathers are more responsive to infant cues than are non-fathers and fathers' responses to infant cues are related to both hormones and to caregiving experience.     

Fatherhood, pairbonding and testosterone in the Philippines

In species with a high level of paternal care, including humans, testosterone (T) is believed to help mediate the trade-off between parenting and mating effort. This hypothesis is supported by the observation of lower T in pairbonded men or fathers compared to single, non-fathers; however, prior work has highlighted population variation in the association between T and pairbonding or fatherhood status. Here we evaluate this hypothesis in a large (n = 890), representative birth cohort of young men (age range 20.5–22.5 years) living in Cebu City, the Philippines. Bioavailable T was measured in saliva collected prior to bed and immediately upon waking the following morning. Plasma T and luteinizing hormone (LH) were measured in morning plasma samples. In this sample, 20% of men were pairbonded, defined as living with a partner or married, 13% were fathers, and roughly half of fathers reported involvement in childcare. Pairbonded men had significantly lower T at both times of day. Unlike in other populations, this relationship was accounted for entirely by fatherhood status: among the large sub-sample of non-fathers, mean T was nearly identical among pairbonded and single men. There was a strong association between self-reported involvement in childcare and lower evening T, supporting the idea that the evening nadir in T is related to social interactions across the day. Similar relationships were found for total plasma T and LH, suggesting that these relationships are coordinated by centrally-mediated changes in LH secretion. The relatively modest T difference in relation to fatherhood at Cebu, in comparison to other studies, may reflect a lower level of paternal involvement in childcare activities in this population. Our findings using a large, well-characterized birth cohort support the hypothesized role of T as a mediator of mating and parenting effort in humans, while contributing evidence for cultural variation in the relative importance of pairbonding and fathering to these relationships.     

Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus

Relatively little is known about hormonal mechanisms underlying paternal behavior in mammals. Male California mice, Peromyscus californicus, display extensive parental care toward their young. Parental behavior of fathers, expectant fathers (males living with their pregnant partner), and virgin males was assessed in a 10-min test with a 1- to 3-day-old alien pup. Few virgin males acted parental (19%) compared to fathers one day postpartum (80%) and expectant fathers (56%). Plasma prolactin levels were significantly elevated in fathers 2 days postpartum compared to expectant fathers and virgin males. Paternal prolactin levels were similar to those of mothers. There were no differences between groups in levels of plasma testosterone. These data suggest, contrary to other reports, that prolactin is a likely correlate of paternal behavior in rodents.     

Steroid Hormone Reactivity in Fathers Watching Their Children Compete

This study examines steroid production in fathers watching their children compete, extending previous research of vicarious success or failure on men’s hormone levels. Salivary testosterone and cortisol levels were measured in 18 fathers watching their children play in a soccer tournament. Participants completed a survey about the game and provided demographic information. Fathers with higher pregame testosterone levels were more likely to report that referees were biased against their children’s teams, and pre- to postgame testosterone elevation was predicted by watching sons compete rather than daughters as well as perceptions of unfair officiating. Pregame cortisol was not associated with pregame testosterone or with perceived officiating bias, but cortisol did fluctuate synergistically with testosterone during spectator competition. Although fathers showed no consistent testosterone change in response to winning or losing, pregame testosterone may mediate steroid hormone reactivity to other aspects of their children’s competition.     

Sensation seeking in fathers: the impact on testosterone and paternal investment

Paternal care is associated with a reduced likelihood of engaging in competitive or mating behavior and an increased likelihood of providing protection when necessary. Over recent years, there has been increasing evidence to assume that the steroid testosterone (T) in men might reflect the degree of mating effort. In line with this, decreased T levels were shown in fathers compared to non-fathers and it was suggested that paternal care, and most behavior positively associated with T, might be incompatible with each other. Independently, the personality trait sensation seeking (SS) has been related to mating behavior and also to elevated T in men. Aiming to integrate these different lines of research in a longitudinal approach, we explored the impact of SS on T levels in the context of the transition to fatherhood. Thirty-seven fathers and 38 men without children but in committed, romantic relationships (controls) were recruited. At two time points (for fathers: four weeks prior to (t1) and eight weeks after birth (t2)), all subjects repeatedly collected saliva samples for T measurement, filled in a protocol of activities during the course of these days and completed an online questionnaire. In line with our hypotheses, the results show significantly lower aggregated (AUC-T) T levels in fathers compared with non-fathers. Furthermore, moderation analyses revealed a significant interaction between group and SS at t2, with the lowest T levels in low SS fathers. These data suggest that adaptation processes of the transition to fatherhood are influenced by individual differences in personality traits.     

Selective increase in plasma luteinising hormone concentrations in drug free young men with mania.

The hypothalamic-pituitary-gonadal system was investigated in drug free young men with either mania or acute schizophrenia and in age matched controls by measuring, at frequent intervals during a 17 hour "neuroendocrine day," plasma concentrations of luteinising hormone (LH), follicle stimulating hormone, prolactin, testosterone, sex hormone binding globulin (SHBG), and cortisol. Plasma LH in mania was significantly increased compared with the control value at all time periods and increased in the morning and evening samples compared with values in the schizophrenic patients. Plasma prolactin and cortisol concentrations were significantly greater in mania and schizophrenia compared with control values at several times during the day, but there were no significant between group differences in plasma testosterone or SHBG. These results show that in young men with mania there is a major disturbance in the central mechanisms that control the release of LH, the control of prolactin and cortisol secretion is abnormal in mania and acute schizophrenia, and plasma LH concentrations may provide a useful hormonal diagnostic test for mania.     

Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons

Magnocellular neurons of the supraoptic (SON) and paraventricular nuclei (PVN) show considerable plasticity during pregnancy and lactation. Prolactin receptors (PRL-R) have been identified in both these nuclei. The aim of this study was to investigate the cell type(s) expressing mRNA for the long form of prolactin receptor (PRL-R(L)) and to determine whether patterns of expression change during pregnancy and lactation. In addition, we examined effects of prolactin on excitability of oxytocin and vasopressin neurons. Sections from brains of nonpregnant, pregnant, and lactating rats were hybridized with an 35S-labeled probe to label PRL-R(L) mRNA together with digoxigenin-labeled probes to detect either oxytocin or vasopressin mRNA. In the SON, PRL-R(L) mRNA was predominantly colocalized with oxytocin mRNA, with over 80% of oxytocin neurons positive for PRL-R(L) mRNA. Very few (<10%) vasopressin neurons expressed PRL-R(L) mRNA. In the PVN, PRL-R(L) mRNA was also predominantly found in oxytocin neurons, and the proportion of PRL-R(L)-positive oxytocin neurons increased significantly during pregnancy and lactation. As in the SON, relatively few vasopressin cells contained PRL-R(L) mRNA. For in vivo electrophysiology, nonpregnant rats were anesthetized, and then extracellular single neuron activity was recorded in identified oxytocin and vasopressin neurons. After a period of baseline recording, the effect of prolactin (1 microg i.c.v.) on firing rate was examined. Prolactin treatment of nonpregnant rats induced a significant decrease in firing rates of oxytocin neurons. There was no effect of prolactin on the activity of vasopressin neurons. Together, these data provide strong evidence that prolactin directly and specifically regulates activity of oxytocin neurons.     

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.     

Plasma galanin, vasopressin, and oxytocin in patients with Addison's disease.

Galanin is colocalized with adrenocorticotrophin (ACTH) in the human pituitary and with corticotrophin releasing hormone, arginine, vasopressin, and oxytocin in the hypothalamus. Galanin, vasopressin, and oxytocin influence the secretion of pituitary ACTH. The aim of this study was to investigate if the endogenous stimulation of ACTH release in Addison's disease was reflected in plasma galanin, vasopressin, and oxytocin. ACTH, galanin, vasopressin, and oxytocin were measured in plasma from 14 patients with Addison's disease, one patient with Nelson's syndrome, and 14 healthy controls. Eight patients had elevated plasma ACTH whereas six patients and all controls had ACTH levels within the reference-range. There was no difference in galanin or vasopressin between patients and controls or between samples with low or high ACTH concentrations. In contrast, oxytocin was higher in patients with elevated plasma ACTH compared to patients and controls with normal or low ACTH. No relation was found between galanin or oxytocin and age or sex. A tendency towards lower vasopressin with increasing age was found among the men (p=0.057). The highest ACTH and galanin levels were found in the patient with Nelson's syndrome. In conclusion, increased plasma ACTH was not reflected in elevated plasma galanin or vasopressin. In contrast, elevated ACTH levels were accompanied by higher oxytocin levels.     

Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus)

High levels of prolactin have been found to correlate with the expression of paternal care in a variety of taxa. However, in mammals, there is little experimental evidence that prolactin is causally involved in the stimulation or maintenance of paternal care. Here, we suppressed prolactin production in paternally experienced common marmoset fathers in their family groups during the first 2 weeks after their infants were born. Circulating prolactin levels were suppressed using cabergoline (Dostinex: Pfizer), a long acting dopamine (D2) agonist with minimal behavioural side-effects. A within-subject design was used to compare behavioural and hormonal data on 5 paternally experienced fathers during two consecutive births. Cabergoline reduced prolactin to negligible levels in all fathers without effecting testosterone, DHT and cortisol and without adverse side-effects. However, lowering prolactin had no significant effect on the expression of majority of the behaviour patterns associated with paternal care. These included infant carrying, infant grooming and the frequency with which fathers retrieved and rejected infants. The only infant-related behaviour to be affected was the frequency with which fathers touched, licked and investigated infants. We noted a marginally significant increase in this behaviour during cabergoline treatment. Despite the lack of effect on paternal care, cabergoline did exert an effect on the affiliative/sexual behaviour of fathers as there was a significant increase in the grooming behaviour fathers directed at and received from their mates during drug treatment. This study showed that experienced male marmosets can express paternal behaviour in the absence of the high prolactin levels normally seen after infants are born.     

Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus

Male cotton-top tamarins, Saguinus oedipus, display hormonal changes associated with parenting prior to the birth of their infants. Here we examined the hormonal changes that occurred in experienced and inexperienced fathers during the postconception period, prior to the birth of infants. Noninvasive techniques were used to collect urine from 10 male cotton-top tamarins (5 experienced and 5 inexperienced breeders) three times weekly during the 6-month gestation period. Samples were analyzed for prolactin, testosterone, dihydrotestosterone (DHT), and cortisol, averaged by gestational month. Experienced males showed elevated prolactin during the mate's 3rd gestational month, and the elevation correlated with the number of infants surviving from the previous birth (0, 1, and 2) but not with outcome of the current pregnancy. However, an experienced male with no infants present still showed elevated prolactin and some inexperienced males showed elevated prolactin just before parturition, suggesting noninfant cues are also important. While prolactin levels were influenced by the male's prior infant experience, testosterone levels did not differ between experienced and inexperienced males. Testosterone levels were significantly elevated for all males during the 3rd, 4th and 5th months but had no relationship with number of infants present or with outcome of current pregnancy. DHT decreased during the second half of pregnancy compared with testosterone but this finding was not consistent for every male. No significant changes occurred in cortisol levels. These results suggest that infant-rearing experience affected the hormonal responsitivty of the male to his mate's current pregnancy.     

The effect of mental rotation on changes in plasma testosterone and cortisol levels

Testosterone level has an influence on cognitive functions, especially spatial abilities. The relationship is, however, bidirectional and brain activity also affects testosterone levels. The aim of this study was to analyze the effects of an intensive 3D mental rotation task on testosterone levels in young healthy men and women. In the mental rotation task, men reached a higher top score (P=0.027) and total score (P=0.004) compared to women. In 8 out of 9 women (P=0.008) but not in men (P=0.129) testosterone levels decreased after one hour of mental rotation testing. A significant gender difference was shown (P<0.0001). In all women, plasma cortisol levels was significantly lower after testing (P=0.004). In men cortisol levels decreased in 7 out of 9 subjects (P=0.039). A significant gender difference was not found (P=0.19). No association was found in women between baseline testosterone levels and mental rotation total score (P=0.810). In men there was a positive correlation between baseline testosterone and mental rotation total score (P=0.015). A significant difference gender difference was seen in the association between testosterone and mental rotation score (P<0.05). Mental rotation stimuli caused significant changes in hormonal levels of testosterone and cortisol. A gender-specific response was detected in testosterone fluctuation.     

Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care

Male rodents that are naturally paternal, like all females, must inhibit infanticide and activate direct parental behavior as they become parents. Males, however, alter their behavior in the absence of parturition, postpartum ovulation and lactation, and therefore do not experience the hormone dynamics associated with such conditions. Paternal males might nevertheless use the same hormones to activate pre-existing maternal behavior pathways in the brain. Positive and inverse associations between prolactin, sex steroids (estradiol, testosterone, progesterone), glucocorticoids, oxytocin and vasopressin and paternal behavior are reviewed. Across biparental rodents (Phodopus campbelli, Peromyscus californicus, Microtus ochrogaster, and Meriones unguiculatus), as well as non-human primates and men, hormone-behavior associations are broadly supported. However, experimental manipulations (largely restricted to P. campbelli) suggest that the co-variation of hormones and paternal behavior is not causal in paternal behavior. Perhaps the hormone-behavior associations shared by P. campbelli and other paternal males are important for other challenges at the same time as fatherhood (e.g., mating during the postpartum estrus). On the other hand, each paternal species might, instead, have unique neuroendocrine pathways to parental behavior. In the latter case, future comparisons might reveal extraordinary plasticity in how the brain forms social bonds and alters behavior in family groups.     

Short-term changes in fathers' hormones during father-child play: impacts of paternal attitudes and experience

Hormonal differences between fathers and non-fathers may reflect an effect of paternal care on hormones. However, few studies have evaluated the hormonal responses of fathers after interacting with their offspring. Here we report results of a 30-minute in-home experiment in which Filipino fathers played with their toddlers and consider whether paternal experience and men's perceptions of themselves as fathers affect hormonal changes. Fathers provided saliva and dried blood spot samples at baseline (B) and 30 (P30) and 60 (P60, saliva only) minutes after the interaction. We tested whether testosterone (T), cortisol (CORT), and prolactin (PRL) shifted after the intervention. In the total sample, T did not vary over the study period, while CORT declined from B to P30 and P60, and PRL also declined from B to P30. Fathers who spent more time in daily caregiving and men who thought their spouses evaluated them positively as parental caregivers experienced a larger decline in PRL (B to P30) compared to other fathers. First-time fathers also had larger declines in PRL compared to experienced fathers. Experienced fathers also showed a greater decline in CORT (B to P60) compared to first-time fathers. These results suggest that males' paternal experience and age of offspring affect hormonal responses to father–child play and that there is a psychobiological connection between men's perceptions of themselves as fathers and their hormonal responsivity to childcare.     

Short-term changes in fathers' hormones during father–child play: Impacts of paternal attitudes and experience

Hormonal differences between fathers and non-fathers may reflect an effect of paternal care on hormones. However, few studies have evaluated the hormonal responses of fathers after interacting with their offspring. Here we report results of a 30-minute in-home experiment in which Filipino fathers played with their toddlers and consider whether paternal experience and men's perceptions of themselves as fathers affect hormonal changes. Fathers provided saliva and dried blood spot samples at baseline (B) and 30 (P30) and 60 (P60, saliva only) minutes after the interaction. We tested whether testosterone (T), cortisol (CORT), and prolactin (PRL) shifted after the intervention. In the total sample, T did not vary over the study period, while CORT declined from B to P30 and P60, and PRL also declined from B to P30. Fathers who spent more time in daily caregiving and men who thought their spouses evaluated them positively as parental caregivers experienced a larger decline in PRL (B to P30) compared to other fathers. First-time fathers also had larger declines in PRL compared to experienced fathers. Experienced fathers also showed a greater decline in CORT (B to P60) compared to first-time fathers. These results suggest that males' paternal experience and age of offspring affect hormonal responses to father–child play and that there is a psychobiological connection between men's perceptions of themselves as fathers and their hormonal responsivity to childcare.     

Testosterone levels correlate with the number of children in human males,but the direction of the relationship depends on paternal education

Most research shows that fatherhood is related to reduced testosterone (T) levels, but relationships between the number of children and T levels are not addressed. In humans, paternal care usually involves obtaining adequate resources to support children, which may require engaging in male–male competition and maintaining high T levels. We hypothesize that T levels in fathers should increase with increasing family size. In 78 Polish men, aged 30 to 77 years, the number of children was significantly correlated with paternal T levels, but the direction of this relationship was dependent on the fathers' education. In agreement with our hypothesis, in men with below-college education, T levels increased with increasing number of children. In contrast, in men with college education, the number of children was negatively related to paternal T levels. Drop in T levels throughout the day tended to be less pronounced the more children fathers had, irrespective of their educational level. Our results suggest that a hypothesis of simple trade-offs between mating and parenting effort may be too simplistic to explain changes in testosterone response to parenting in human males. In order to understand functional response of changes in T levels, it is crucial to account for family size and socioeconomic factors. However, due to the cross-sectional study design, we cannot exclude the possibility that T levels influenced reproductive behavior (rather than vice versa) and thus the number of children produced by men.