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.     

Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers

Glucocorticoids are thought to mediate the disruption of parental behavior in response to acute and chronic stress. Previous research supports their role in chronic stress; however, no study has experimentally tested the effects of acute glucocorticoid elevation on paternal behavior. We tested the prediction that acute corticosterone (CORT) increases would decrease paternal behavior in California mouse fathers and would lead to longer-term effects on reproductive success, as even short-term increases in CORT have been shown to produce lasting effects on the hypothalamic-pituitary-adrenal axis. First-time fathers were injected with 30 mg/kg CORT, 60 mg/kg CORT or vehicle, or left unmanipulated. Interactions between the male and its pup(s) were recorded 1.5–2 h after injection and scored for paternal and non-paternal behavior. Treatment groups were combined into control (unmanipulated + vehicle, n = 15) and CORT (30 mg/kg + 60 mg/kg, n = 16) for analysis based on resulting plasma CORT concentrations. CORT treatment did not alter paternal or non-paternal behaviors or any long-term measures (male body mass or temperature, pup growth rate, pup survival, interbirth interval, number or mass of pups born in the second litter). Fathers showed a significant rise in body mass at day 30 postpartum, followed by a decrease in body mass after the birth of the second litter; however, this pattern did not differ between the CORT and control groups. In summary, acute elevation of plasma CORT did not alter direct paternal behavior, body mass, or reproductive outcomes, suggesting that acute CORT elevation alone does not overtly disrupt paternal care in this biparental mammal.     

Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy

In the cotton-top tamarin, a primate where paternal care is critical to the survival of the offspring, we found that expectant fathers experienced multiple hormonal changes during their mate's pregnancy. Fathers that had experienced several previous births showed significant changes in urinary estrogens, androgens, prolactin and cortisol in the last 2 months before birth, whereas less-experienced fathers (LEF) did not. The female's midpregnancy rise in glucocorticoids was followed within 1-2 weeks by a peak of cortisol and corticosterone in her paired male in 70% of all males and 100% of all experienced males. Examination of behavioral interactions between the pairs did not reveal changes in rates of interactions between the experienced pairs over pregnancy. However, the less-experienced pairs had significantly higher levels of affiliative and sexual interactions. Therefore, behavioral communication between the pair did not appear to account for the hormonal changes occurring within the experienced fathers (EF). The midpregnancy rise of glucocorticoids in females may stimulate a glucocorticoid response in male tamarins and thereby activate other hormonal changes in males to prepare them for their parenting role.     

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.     

Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers

Glucocorticoids are thought to mediate the disruption of parental behavior in response to acute and chronic stress. Previous research supports their role in chronic stress; however, no study has experimentally tested the effects of acute glucocorticoid elevation on paternal behavior. We tested the prediction that acute corticosterone (CORT) increases would decrease paternal behavior in California mouse fathers and would lead to longer-term effects on reproductive success, as even short-term increases in CORT have been shown to produce lasting effects on the hypothalamic-pituitary-adrenal axis. First-time fathers were injected with 30 mg/kg CORT, 60 mg/kg CORT or vehicle, or left unmanipulated. Interactions between the male and its pup(s) were recorded 1.5–2 h after injection and scored for paternal and non-paternal behavior. Treatment groups were combined into control (unmanipulated + vehicle, n = 15) and CORT (30 mg/kg + 60 mg/kg, n = 16) for analysis based on resulting plasma CORT concentrations. CORT treatment did not alter paternal or non-paternal behaviors or any long-term measures (male body mass or temperature, pup growth rate, pup survival, interbirth interval, number or mass of pups born in the second litter). Fathers showed a significant rise in body mass at day 30 postpartum, followed by a decrease in body mass after the birth of the second litter; however, this pattern did not differ between the CORT and control groups. In summary, acute elevation of plasma CORT did not alter direct paternal behavior, body mass, or reproductive outcomes, suggesting that acute CORT elevation alone does not overtly disrupt paternal care in this biparental mammal.     

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.     

Paternal Effects on Offspring Fitness Reflect Father’s Social Environment

In many species, males influence phenotypic traits in their offspring through non-genetic paternal effects. Such effects can represent a form of paternal investment, and males may benefit by adjusting the effects depending on environmental parameters, such as operational sex ratio, so as to maximize offspring fitness. In the neriid fly Telostylinus angusticollis, fathers reared on a nutrient-rich larval diet produce larger offspring, independent of the rearing environment of the offspring. Here we asked whether this paternal effect was influenced by the social environment to which fathers were exposed. We found significant interactions of the effects of paternal larval diet quality and social environment (same-sex vs. mixed-sex groups) on offspring fitness-related traits. Fathers reared on a nutrient-rich diet produced larger male offspring when housed in mixed-sex groups. However, fathers reared on a nutrient-rich diet produced more viable offspring (or more viable sperm) when housed in same-sex groups prior to mating. These results suggest that fitness-enhancing paternal effects can trade off, consistent with parental investment theory on the offspring size-number trade-off, which suggests that these traits represent alternative investment options and parents are selected to optimize the balance based on a range of environmental variables. This is the first study to show that males can facultatively modulate paternal effects based on the social environment.     

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

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

Does Cosleeping Contribute to Lower Testosterone Levels in Fathers? Evidence from the Philippines

Because cross-species evidence suggests that high testosterone (T) may interfere with paternal investment, the relationships between men''s transition to parenting and changes in their T are of growing interest. Studies of human males suggest that fathers who provide childcare often have lower T than uninvolved fathers, but no studies to date have evaluated how nighttime sleep proximity between fathers and their offspring may affect T. Using data collected in 2005 and 2009 from a sample of men (n = 362; age 26.0 ± 0.3 years in 2009) residing in metropolitan Cebu, Philippines, we evaluated fathers'' T based on whether they slept on the same surface as their children (same surface cosleepers), slept on a different surface but in the same room (roomsharers), or slept separately from their children (solitary sleepers). A large majority (92%) of fathers in this sample reported practicing same surface cosleeping. Compared to fathers who slept solitarily, same surface cosleeping fathers had significantly lower evening (PM) T and also showed a greater diurnal decline in T from waking to evening (both p<0.05). Among men who were not fathers at baseline (2005), fathers who were cosleepers at follow-up (2009) experienced a significantly greater longitudinal decline in PM T over the 4.5-year study period (p<0.01) compared to solitary sleeping fathers. Among these same men, baseline T did not predict fathers'' sleeping arrangements at follow-up (p>0.2). These results are consistent with previous findings indicating that daytime father-child interaction contributes to lower T among fathers. Our findings specifically suggest that close sleep proximity between fathers and their offspring results in greater longitudinal decreases in T as men transition to fatherhood and lower PM T overall compared to solitary sleeping fathers.     

Development of prolactin levels in marmoset males: from adult son to first-time father

Previous studies have found a clear relationship between prolactin (prl) and paternal care in various vertebrate taxa. In New World monkeys, it has been demonstrated in several species that fathers have high prolactin levels even during periods without infant rearing. In this study, we followed the reproductive careers of common marmoset males as they transitioned from being an adult son within their native family to fathering their own offspring for the first time. Specifically, we examined the first experience of elevated prolactin levels in marmoset males. Additionally, we investigated the effects of the total number of experienced births as well as of age on prolactin levels. Our results show that common marmoset males did not experience an increase in prolactin secretion after pairing or shortly before birth of their first infants. However, prolactin levels rose more than twofold after the birth of their first infants and had lowered again 2.5 months after this event. We found no correlation between prolactin levels and the number of previous births experienced or age. Our study demonstrates that further work about a possible enhancing effect of prolactin on paternal care, by means of experimentally reducing hormonal levels, should be conducted in common marmosets using first-time fathers before males experience the first paternal increase in prolactin levels.     

Testosterone and Jamaican Fathers

This paper investigates relationships between men’s testosterone and family life in a sample of approximately 350 Jamaican fathers of children 18–24 months of age. The study recognizes the role of testosterone as a proximate mechanism coordinating and reflecting male life history allocations within specific family and cultural contexts. A sample of Jamaican fathers and/or father figures reported to an assessment center for an interview based on a standardized questionnaire and provided a saliva sample for measuring testosterone level. Outcomes measured include subject demographics such as age and relationship status as well as partnership quality and sexuality and paternal attitudes and behavior. The variation in these fathers’ relationship status (e.g., married co-residential fathers, fathers in new non-residential relationships) was not associated with men’s testosterone. Too few stepfathers participated to enable a direct test of the prediction that stepfathers would have higher testosterone than biological fathers, although fathers who reported living with partners’ (but not his own) children did not have higher testosterone than fathers not reporting residing with a non-biological child. Fathers’ relationship quality was negatively related to their testosterone. Measures of paternal attitudes and behavior were not related to fathers’ testosterone. Consistent with previous ethnography, this sample of Jamaican fathers exhibited variable life history profiles, including residential status. We discuss why fathers’ relationship quality was found to be negatively related to their testosterone level, but other predictions were not upheld.     

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 and paternal care in East African foragers and pastoralists

The 'challenge hypothesis' posits that testosterone facilitates reproductive effort (investment in male-male competition and mate-seeking) at the expense of parenting effort (investment in offspring and mates). Multiple studies, primarily in North America, have shown that men in committed relationships, fathers, or both maintain lower levels of testosterone than unpaired men. Data from non-western populations, however, show inconsistent results. We hypothesized that much of this cross-cultural variation can be attributed to differential investment in mating versus parenting effort, even among married fathers. Here, we directly test this idea by comparing two neighbouring Tanzanian groups that exhibit divergent styles of paternal involvement: Hadza foragers and Datoga pastoralists. We predicted that high levels of paternal care by Hadza fathers would be associated with decreased testosterone in comparison with non-fathers, and that no such difference between fathers and non-fathers would be evident in Datoga men, who provide minimal direct paternal care. Twenty-seven Hadza men and 80 Datoga men between the ages of 17 and 60 provided morning and afternoon saliva samples from which testosterone was assayed. Measurements in both populations confirmed these predictions, adding further support to the hypothesis that paternal care is associated with decreased testosterone production in men.     

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.     

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.     

Early life of fathers affects offspring fitness in a wild rodent

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These nongenetic, environment‐dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, to test the hypothesis that a high population density environment in the early life of fathers can affect traits associated with offspring fitness. We show that the protein content in the diet and/or social environment experienced during the father's early life (prenatal and weaning) influence the phenotype and survival of his offspring and may indicate adaptation to density‐dependent costs. Furthermore, we show that experiencing multiple environmental factors during the paternal early life can lead to a different outcome on the offspring phenotype than stimulated by experience of a single environmental factor, highlighting the need to study developmental experiences in tandem rather than independent of each other.     

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.     

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

In many animals, including humans, interactions with caring parents can have long-lasting effects on offspring sensitivity to stressors. However, whether these parental effects impact offspring fitness in nature is often unclear. In addition, despite evidence that maternal care can influence offspring behaviour via epigenetic alterations to the genome, it remains unclear whether paternal care has similar effects. Here, we show in three-spined sticklebacks, a fish in which fathers are the sole provider of offspring care, that the direct care provided by fathers affects offspring anxiety and the potential for epigenetic alterations to the offspring genome. We find that families are differentially vulnerable to early stress and fathers can compensate for this differential sensitivity with the quality of their care. This variation in paternal care is also linked to the expression in offspring brains of a DNA methyltransferase (Dnmt3a) responsible for de novo methylation. We show that these paternal effects are potentially adaptive and anxious offspring are unlikely to survive an encounter with a predator. By supplying offspring care, fathers reduce offspring anxiety thereby increasing the survival of their offspring—not in the traditional sense through resource provisioning but through an epigenetic effect on offspring behavioural development.     

Relative and combined effects of estradiol and prolactin on corticosterone secretion in ovariectomized rats

In vivo and in vitro experiments were designed to assess the relationship of the estradiol (E2) and prolactin (PRL) on glucocorticoid secretion in ovariectomized (Ovx) rats. Female rats were Ovx for two weeks and then subcutaneously injected with oil or estradiol benzoate (EB) for 3 days before experimentation. Venous blood samples were collected from right jugular vein at 0, 30, 60, 90, and 120 min after challenge with adrenocorticotropin (ACTH). Adrenal zona fasciculata-reticularis (ZFR) cells from Ovx rats were isolated and incubated with E2 or PRL. In the morning and afternoon, EB enhanced the basal and ACTH-stimulated concentrations of plasma corticosterone (CORT) and PRL. Administration of E2 in vitro increased the basal and ACTH-stimulated release of CORT and production of adenosine 3', 5'-cyclic monophosphate (cAMP) in ZFR cells. E2 enhanced the forskolin-stimulated release of CORT by ZFR cells. However, the 3-isobutyl-l-methylxanthine (IBMX)- or 8-Br-cAMP-stimulated release of CORT was not affected by E2. E2 augmented the lower doses of PRL-stimulated release of CORT and cAMP accumulation as compared with the PRL-treated group alone. Incubation of higher doses of PRL increased the production of cAMP. Administration of nifedipine and R(+) BK8644 (classic L-type Ca2+ channel blocker) significantly attenuated the PRL-stimulated release of CORT. Taken together, these data indicate that E2- and PRL-related increase of CORT in Ovx rats is associated with the increase of cAMP accumulation and calcium influx in ZFR cells. In conclusion, E2 and PRL play a stimulatory role in the co-regulation of CORT secretion.     

Paternity cues and mating opportunities: what makes fathers good?

Human males provide facultative paternal investment to their offspring; that is, the male care is not necessary for the survival of his offspring. It is expected that the degree of male investment (1) increases with growing paternity certainty, (2) increases when investment increases the survival and later reproductive prospect of offspring and (3) declines when there are opportunities to mate with multiple females. Using a large sample of adult offspring and their fathers (n = 245), we first investigated the role of two factors possibly involved in the assessment of paternity and subsequently regulating the level of paternal investment: (a) father–child facial resemblance and (b) assortative mating for eye colour. Second, because mating opportunities are inversely related to paternal investment, we also investigated how male facial attractiveness (a cue of mate opportunities) correlates with paternal investment. In line with paternal investment theory, male investment positively correlated with offspring facial resemblance. However, paternal investment were neither higher among blue-eyed couples, nor there were preferences of blue-eyed men to marry with blue-eyed women. Moreover, father facial attractiveness was unrelated to paternal investment. These results indicate that resemblance between offspring and their fathers still plays an important role in paternal investment decision later in offspring’s life.