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.     

Oxytocin changes primate paternal tolerance to offspring in food transfer

Oxytocin facilitates social recognition in rats and mice, onset of maternal behavior in virgin mice and formation of pair bonds without copulation in prairie voles. However, the relationship between this peptide and paternal behavior in primates remains largely unknown. We investigated whether oxytocin affects paternal behavior in common marmosets. In these primates, fathers as well as mothers take care of their infants, and transferring food to the infants is one of their more obvious caretaking behaviors. We tested whether oxytocin and an oxytocin receptor antagonist affect the transfer of food to offspirng by fathers. After intracerebroventricular infusion of the vehicle, oxytocin, or the oxytocin receptor antagonist, the fathers’ behavior, including picking up food, transferring food to the offspring, and refusing to transfer food to the offspring, was analyzed. Compared with the vehicle, oxytocin reduced the frequency of refusal. This was not caused by reduction of appetite. Although the oxytocin receptor antagonist did not change the frequency of refusal behavior of the fathers statistically significant manner, these observations suggest that the tolerance of the adult male marmoset toward its offspring as shown by the transfer of food is increased by oxytocin administered into the central nervous system.     

Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters, Phodopus campbelli

Male Djungarian hamsters, Phodopus campbelli, are highly parental and experience a late-afternoon prolactin surge before the birth that is not seen in a closely related species, P. sungorus, which lacks paternal care. At the same stage, female prolactin is needed for later maternal behavior. Male prolactin was suppressed in first-time fathers before the birth of the litter using two different dopamine agonists, bromocriptine mesylate and cabergoline. Plasma prolactin concentration confirmed the efficacy of each treatment. Paternal responsiveness was quantified using three variations on a pup-displacement paradigm. No adverse effects of either treatment were seen. Across four experiments, there was no decrease in paternal retrieval or in retrieval latency in response to male prolactin suppression. In addition, there was no decrease in litter growth or survival, nor was there an increase in maternal investment to compensate for a deficit in paternal care. As cabergoline suppression of prolactin persisted after the birth without behavioral deficits, prolactin after the birth was also not required for the expression of paternal behavior. In spite of an extensive literature supporting an association between prolactin and natural paternal behavior, we conclude that dopamine-mediated prolactin release into peripheral plasma is not essential for paternal responsiveness in P. campbelli.     

The role of fathers in mammalian sex allocation

Parents should bias resource allocation towards the sex most likely to provide higher fitness returns by adjusting the birth sex ratio and/or through differential care of sons and daughters. Sex allocation research in mammals to date has been focused almost exclusively on maternal traits, but fathers may also play an important role. Future studies should investigate the influence of paternal quality on the fitness of sons and daughters, and possible conflicts of interest between mothers and fathers. There is also a crucial need for more studies examining whether relative levels of maternal care in sons and daughters depend on paternal quality.     

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.     

Hormonal correlates of human paternal interactions: a hospital-based investigation in urban Jamaica

To expand our understanding of the neuroendocrine mechanisms underlying human fatherhood, including its cross-cultural expression, we investigated the hormonal correlates of fatherhood in the greater Kingston, Jamaica area. We recruited 43 men, aged 18-38, to participate: 15 single men; 16 "coresidential" fathers (men who live with their adult female partner and youngest child); and 12 "visiting" fathers (men who live apart from their adult female partner and youngest child). The research protocol entailed biological sampling before and after a 20-min behavioral session during which single men sat alone and fathers interacted with their partner and youngest child. Hormone measures relied upon minimally invasive techniques (salivary testosterone and cortisol, finger prick blood spot prolactin, urinary oxytocin and vasopressin). Results revealed significant group differences in average male testosterone levels (p=0.006), with post hoc contrasts indicating that visiting fathers had significantly (p<0.05) lower testosterone levels than single men. Prolactin profiles also differed significantly across groups (p=0.010) whereby post hoc contrasts showed that prolactin levels of single men declined significantly compared with the flat levels of visiting fathers (p<0.05). No group differences in cortisol, oxytocin or vasopressin levels were observed. However, among fathers, vasopressin levels were significantly and negatively (r=-.431, p=0.022) correlated with the age of a man's youngest child. These results thus implicate lower testosterone levels as well as prolactin and vasopressin in human fatherhood. These findings also highlight the importance of sociocultural context in human fatherhood while exhibiting parallels with existing data on the non-human vertebrate hormonal bases of paternal care.     

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.     

Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii)

We describe temporal patterns of change in paternal behaviour and urinary concentrations of the steroid hormones testosterone (T) and oestradiol (E(2)) in male black tufted-ear marmosets, Callithrix kuhlii, relative to the birth of their young, and test predictions of the hypotheses that (1) high levels of T are incompatible with paternal care and (2) levels of T and E(2)vary with a father's prior experience in his family group. After young were born, levels of urinary T and E(2)remained near prepartum concentrations and rates at which fathers carried infants were below peak levels until the approximate time that postpartum mating ordinarily occurs, suggesting a possible trade-off between readiness to mate and paternal behaviour in C. kuhlii. Infant-carrying behaviour of fathers occurred at its highest rate 3-4 weeks after parturition and coincided with significant declines in urinary levels of T and E(2), providing preliminary support for the hypothesis that these hormones are antagonistic to paternal behaviour. Urinary T and E(2)declined among fathers regardless of whether their young survived to weaning or died at birth, indicating that variation in these hormones after parturition occurs even in the absence of continued stimuli from infants. When adjusted for declines ordinarily associated with aging, urinary T tended to be lower among fathers with a great deal of prior experience caring for young compared with fathers having little or no experience, suggesting that either experience affects T levels of fathers, or that T levels influence fathers' chances of successfully rearing infants. Overall, our results suggest that in male C. kuhlii, T, and possibly E(2), play an important role in balancing the expression of paternal care with that of other reproductive behaviours. Copyright 2000 The Association for the Study of Animal Behaviour.     

Parental responsiveness negatively correlates with fecal testosterone concentration in male mandarin voles (Microtus mandarinus)

The tradeoff between parental effort and mating effort in male animals may be mediated by testosterone (T). The pattern of association between T and paternal care in birds is consistent with this hypothesis, while it is poorly studied and not universal for mammals. We used the correlation approach to test two predictions of T-mediated tradeoff hypothesis for a biparental vole, Microtus mandarinus: (1) that T levels in males decrease from before pair formation to after birth of the first litter and (2) that paternal responsiveness of males negatively correlates with their T levels. T concentrations were measured in fecal samples collected before pairing and then immediately before behavioral testing on day 5 after birth of the first litter. Both nonpaternal and low paternal males had high initial T that decreased after birth of pups, though the decrease was only significant in low paternal males. In highly paternal males, the initial T was low and did not change after birth. Our results support the predictions of T-mediated tradeoff hypothesis and reveal individual variation in hormone–behavior relationship.     

Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels

In monogamous mammals paternal care plays an important role in the neural and behavioral development of offspring. However, the neuroendocrine mechanisms underlying paternal behavior remain poorly understood. Here, we investigate the association between natural variation in paternal responsiveness and central levels of oxytocin (OT) and estrogen receptor alpha (ERα). We used the frequency of licking and grooming behavior to distinguish low paternal responsiveness and high paternal responsiveness in virgin mandarin voles (Microtus mandarinus). Males that engaged in high paternal behavior had elevated levels of OT immunoreactive neurons in the paraventricular nuclei of the hypothalamus and supraoptic nuclei of the hypothalamus compared with males that displayed low paternal behavior. Likewise, males of high paternal responsiveness had more ERα immunoreactive neurons in the medial preoptic area, bed nucleus of the stria terminalis, arcuate nucleus of the hypothalamus and medial amygdaloid nucleus compared to low responsive males. The level of ERα immunoreactive neurons in the ventromedial hypothalamic nucleus was lower in highly paternal males compared to less paternal males. These results suggest that natural variation in paternal responsiveness may be directly related to variation in central OT and ERα.     

From here to paternity: Neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus)

In a minority of mammalian species, including humans, fathers play a significant role in infant care. Compared to maternal behavior, the neural and hormonal bases of paternal care are poorly understood. We analyzed behavioral, neuronal and neuropeptide responses towards unfamiliar pups in biparental California mice, comparing males housed with another male (“virgin males”) or with a female before (“paired males”) or after (“new fathers”) the birth of their first litter. New fathers approached pups more rapidly and spent more time engaging in paternal behavior than virgin males. In each cage housing two virgin males, one was spontaneously paternal and one was not. New fathers and paired males spent more time sniffing and touching a wire mesh ball containing a newborn pup than virgin males. Only new fathers showed significantly increased Fos-like immunoreactivity in the medial preoptic nucleus (MPO) following exposure to a pup-containing ball, as compared to an empty ball. Moreover, Fos-LIR in the bed nucleus of the stria terminalis (STMV and STMPM) and caudal dorsal raphe nucleus (DRC) was increased in new fathers, independent of test condition. No differences were found among the groups in Fos-LIR in oxytocinergic or vasopressinergic neurons. These results suggest that sexual and paternal experiences facilitate paternal behavior, but other cues play a role as well. Paternal experience increases Fos-LIR induced by distal pup cues in the MPO, but not in oxytocin and vasopressin neurons. Fatherhood also appears to alter neurotransmission in the BNST and DRC, regions implicated in emotionality and stress-responsiveness.     

AVPR1b variation and the emergence of adaptive phenotypes in Platyrrhini primates

Platyrrhini (New World monkeys, NWm) are a group of primates characterized by behavioral and reproductive traits that are otherwise uncommon among primates, including social monogamy, direct paternal care, and twin births. As a consequence, the study of Platyrrhine primates is an invaluable tool for the discovery of the genetic repertoire underlying these taxon‐specific traits. Recently, high conservation of vasopressin (AVP) sequence, in contrast with high variability of oxytocin (OXT), has been described in NWm. AVP and OXT functions are possible due to interaction with their receptors: AVPR1a, AVPR1b, AVPR2, and OXTR; and the variability in this system is associated with the traits mentioned above. Understanding the variability in the receptors is thus fundamental to understand the function and evolution of the system as a whole. Here we describe the variability of AVPR1b coding region in 20 NWm species, which is well‐known to influence behavioral traits such as aggression, anxiety, and stress control in placental mammals. Our results indicate that 4% of AVPR1b sites may be under positive selection and a significant number of sites under relaxed selective constraint. Considering the known role of AVPR1b, we suggest that some of the changes described here for the Platyrrhini may be a part of the genetic repertoire connected with the complex network of neuroendocrine mechanisms of AVP–OXT system in the modulation of the HPA axis. Thus, these changes may have promoted the emergence of social behaviors such as direct paternal care in socially monogamous species that are also characterized by small body size and twin births.     

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.     

Association of paternal age with prevalence of selected birth defects

BACKGROUND: Unlike maternal age, the effect of paternal age on birth defect prevalence has not been well examined. We used cases from the Texas birth defect registry, born during 1996-2002, to evaluate the association of paternal age with the prevalence of selected structural birth defects. METHODS: Poisson regression was used to calculate prevalence ratios (PRs) and 95% confidence intervals (CIs) associated with paternal age for each birth defect, adjusting for maternal age, race/ethnicity, and parity. RESULTS: Relative to fathers ages 25-29 years, fathers 20-24 years of age were more likely to have offspring with gastroschisis (PR 1.47, 95% CI: 1.12-1.94), and fathers 40+ years old were less likely to have offspring with trisomy 13 (PR 0.40, 95% CI: 0.16-0.96). No association was seen between paternal age and prevalence of anencephaly and encephalocele. A selection bias was observed for the other birth defects in which cases of younger fathers were more often excluded from study. CONCLUSIONS: In studies of birth defect risk and paternal age, the source of information may affect the validity of findings.     

Isotocin regulates paternal care in a monogamous cichlid fish

While the survival value of paternal care is well understood, little is known about its physiological basis. Here we investigate the neuroendocrine contributions to paternal care in the monogamous cichlid, Amatitlania nigrofasciata. We first explored the dynamic range of paternal care in three experimental groups: biparental males (control fathers housed with their mate), single fathers (mate removed), or lone males (mate and offspring removed). We found that control males gradually increase paternal care over time, whereas single fathers increased care immediately after mate removal. Males with offspring present had lower levels of circulating 11-ketotestosterone (11-KT) yet still maintained aggressive displays toward brood predators. To determine what brain regions may contribute to paternal care, we quantified induction of the immediate early gene c-Fos, and found that single fathers have more c-Fos induction in the forebrain area Vv (putative lateral septum homologue), but not in the central pallium (area Dc). While overall preoptic area c-Fos induction was similar between groups, we found that parvocellular preoptic isotocin (IST) neurons in single fathers showed increased c-Fos induction, suggesting IST may facilitate the increase of paternal care after mate removal. To functionally test the role of IST in regulating paternal care, we treated biparental males with an IST receptor antagonist, which blocked paternal care. Our results indicate that isotocin plays a significant role in promoting paternal care, and more broadly suggest that the convergent evolution of paternal care across vertebrates may have recruited similar neuroendocrine mechanisms.     

Effects of repeated pup exposure on behavioral,neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus)

In biparental mammals, the factors facilitating the onset of male parental behavior are not well understood. While hormonal changes in fathers may play a role, prior experience with pups has also been implicated. We evaluated effects of prior exposure to pups on paternal responsiveness in the biparental California mouse (Peromyscus californicus). We analyzed behavioral, neural, and corticosterone responses to pups in adult virgin males that were interacting with a pup for the first time, adult virgin males that had been exposed to pups 3 times for 20 min each in the previous week, and new fathers. Control groups of virgins were similarly tested with a novel object (marble). Previous exposure to pups decreased virgins' latency to approach pups and initiate paternal care, and increased time spent in paternal care. Responses to pups did not differ between virgins with repeated exposure to pups and new fathers. In contrast, repeated exposure to a marble had no effects. Neither basal corticosterone levels nor corticosterone levels following acute pup or marble exposure differed among groups. Finally, Fos expression in the medial preoptic area, ventral and dorsal bed nucleus of the stria terminalis was higher following exposure to a pup than to a marble. Fos expression was not, however, affected by previous exposure to these stimuli. These results suggest that previous experience with pups can facilitate the onset of parental behavior in male California mice, similar to findings in female rodents, and that this effect is not associated with a general reduction in neophobia.     

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.     

Experience-facilitated improvements in pup retrieval; evidence for an epigenetic effect

The quality and quantity of maternal care received during infancy are highly predictive of successful infant development. It has been well established, primarily in rats, that the combination of hormonal and infant stimuli at birth modifies neural circuits that regulate maternal responsiveness. During subsequent interactions, infant stimuli are more likely to elicit rapid maternal responsiveness. Some species, such as humans, can display maternal care in the absence of the endocrine events of pregnancy and birth. Similarly, virgin C57BL/6J female mice, display maternal care toward infants, and experience with infants elicits long-lasting increases in maternal care. We hypothesized that these experience-induced changes in behavior may be mediated by chromatin modifications, which in turn change expression of genes that promote maternal care. One site of action is the medial preoptic area (MPOA). To test our hypothesis we treated virgin female mice with sodium butyrate, a histone deacetylase inhibitor. This treatment potentiated maternal responsiveness as well as the expression of several genes: estrogen receptor β (Esr2), oxytocin (Oxt), and cyclicAMP response element binding protein (CREB) binding protein (Crebbp; a histone acetyltransferase) in the MPOA. These data suggest that experience induces high levels of maternal care via epigenetic modifications.     

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.     

Implications of Advancing Paternal Age: Does It Affect Offspring School Performance?

Average paternal age is increasing in many high income countries, but the implications of this demographic shift for child health and welfare are poorly understood. There is equivocal evidence that children of older fathers are at increased risk of neurodevelopmental disorders and reduced IQ. We therefore report here on the relationship between paternal age and a composite indicator of scholastic achievement during adolescence, i.e. compulsory school leaving grades, among recent birth cohorts in Stockholm County where delayed paternity is notably common. We performed a record-linkage study comprising all individuals in Stockholm County who finished 9 years of compulsory school from 2000 through 2007 (n = 155,875). Data on school leaving grades and parental characteristics were retrieved from administrative and health service registers and analyzed using multiple linear regression. Advancing paternal age at birth was not associated with a decrease in school leaving grades in adolescent offspring. After adjustment for year of graduation, maternal age and parental education, country of birth and parental mental health service use, offspring of fathers aged 50 years or older had on average 0.3 (95% CI −3.8, 4.4) points higher grades than those of fathers aged 30–34 years. In conclusion, advancing paternal age is not associated with poorer school performance in adolescence. Adverse effects of delayed paternity on offspring cognitive function, if any, may be counterbalanced by other potential advantages for children born to older fathers.