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.     

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.     

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infant's birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both.     

Prolactin's mediative role in male parenting in parentally experienced marmosets (Callithrix jacchus)

Prolactin has been implicated in promoting paternal care behaviors but little evidence of causality has been found to date except for birds and fish. This study was designed to examine the possible causal relationships between prolactin and male parenting behaviors, reproductive hormones, and physical changes in cooperatively breeding common marmosets, Callithrix jacchus. Fifteen parentally experienced fathers were studied over three consecutive infant care periods during two weeks prior and three weeks following their mates' parturition under three-treatment conditions: normal control pregnancy, decreased prolactin and elevated prolactin. The treatments significantly altered the serum prolactin levels in the fathers. Using three methods of determining a father's level of parental care: infant carrying, family effort and responsiveness to infant stimulus tests, we found that only the male response to infant stimuli was altered by the hormone treatments. Lowering prolactin significantly reduced male responsiveness to infant stimuli but elevating prolactin showed the same effect. Hormonal sampling indicated that testosterone levels showed an inverse relationship to prolactin levels during a normal peripartum period and prolactin treatment reduced this relationship. Prepartum estradiol levels were significantly elevated during the lowered prolactin treatment and estradiol was significantly lowered postpartum with the elevated prolactin treatment. Father's weight decreased significantly by the third week of infant care during the normal treatment. Males in the elevated prolactin treatment lost little or no weight from prepartum while in the lowered prolactin treatment showed the most weight loss. The present findings did not distinguish a direct causal relationship of prolactin on behavior in experienced fathers but did find an interaction with other hormones and weight gain.     

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.     

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.     

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

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.     

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.     

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.     

Direct paternal care in black-and-white snub-nosed monkeys

Mothers of many colobines permit other females or juveniles to have contact with their infants, but paternal care has rarely been reported. This paper reports paternal care in free-ranging black-and-white snub-nosed monkeys Rhinopithecus bieti an endangered and little-known high-altitude species. Direct infant care, carrying or grooming infants, was observed in 2115 of 3988 infant behavioral samples, and 30 of these observations involved direct paternal care. Yearly paternal care was 1.63%, with highest rates in February and March. Monthly paternal care was negatively correlated with infant age, food availability and ambient temperature. Thus, energetic stress may be selective pressure favoring paternal care.     

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.     

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

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

Differential endocrine responses to infant odors in common marmoset (Callithrix jacchus) fathers

Olfactory cues can exert priming effects on many mammalian species. Paternally experienced marmosets, Callithrix jacchus, exposed to direct isolated olfactory contact with their own infant's scent show rapid decreases in testosterone levels within 20 min, whereas paternally inexperienced males do not. The following study tests whether there is a differential steroid response to exposure of infant scent from dependent infants (own and novel) and independent infants (own and novel). We examined the serum levels of estradiol, estrone, testosterone, dihydrotestosterone (DHT), and combined estrogens and androgens in eight male marmosets 20 min after exposure to isolated infant scent. Testosterone and androgen levels combined were significantly lower with exposure to own infant scent than a novel infant scent when the infants were at a dependent age but not at an independent age. Estrogen levels elevated significantly in response to own infant scent when the infants were at a dependent age but not at an independent age. These results suggest that marmoset fathers are more responsive to priming cues from related infants and hormonal responses from fathers are greatest when the infant is at a dependent age.     

Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): interactions with gender, androgen levels, and parenting

Unlike biparental bird and rodent species, mating and parenting occur simultaneously in cotton-top tamarins, Saguinus oedipus, providing a unique model for examining endocrine interactions. This study was designed to determine the relationship of prolactin to testicular androgens during parenting and mating. Specifically we examined (1) the patterns of postpartum prolactin excretion in male and female tamarins with and without infant survival; (2) the relationship between androgen and prolactin levels during the periparturitional period in male tamarins; and (3) male hormonal response to the postpartum mating that occurs simultaneously with paternal care. All females showed an elevation in prolactin during the first week postpartum and when infants died, female prolactin levels decreased significantly. Infant survival during the first 15 days did not influence male levels of prolactin, cortisol, or the testicular androgens testosterone and dihydrotestosterone (DHT). Prolactin did not show an inverse relationship with any of the androgens (testosterone, DHT) studied during the postpartum period. No significant differences in hormones were found between prepartum levels and the first, second, and third 5-day blocks postpartum for all 10 males. Males who had infant-care experience showed an increase in testosterone during the first 5 days postpartum and prolactin levels correlated with the number of previous births a male had experienced. However, the most significant changes in testosterone occurred in males whose mates ovulated during the first 15 days following birth in contrast to males whose mates ovulated later than 15 days. These results indicate that unlike females, male tamarins are not showing hormonal changes in response to infants. Urinary androgens did not show an inverse relationship to prolactin in male tamarins, but were elevated concurrent with the female's fertile period.     

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.     

Social dynamics and individual plasticity of infant care behavior in cooperatively breeding cotton‐top tamarins

Individual variation in infant caretaking behavior is prevalent among marmoset and tamarin monkeys. Although most group members participate in infant care, the timing and amount provided differs greatly. In this study, we quantified general trends in infant carrying behavior by using a longitudinal database that included 11 years of instantaneous scan observations following 80 births of cotton‐top tamarins. Using detailed focal observations on a subset of the same families (10 births) we identified influences that affected expression of infant care at the group and individual levels. Fathers were the primary carriers and paternal carry time gradually decreased with increasing infant age. Paternal carry time also decreased significantly with an increasing number of older sibling helpers. Most fathers began to carry on the first day postpartum. However, we report circumstances in which fathers delayed carrying until almost a month postpartum. Fathers retrieved infants the most, although adult brothers' rates of retrievals peaked and surpassed fathers' rates during week 4 postpartum. Fathers delayed rejection of infants until week 4, whereas mothers rejected infants immediately and throughout the eight weeks. Nonetheless, infants climbed onto their mothers more than onto any other family member. Mothers showed a high initial investment in carrying during the first two weeks, decreasing quickly thereafter. Maternal contributions to infant carrying remained low and relatively consistent regardless of group size. However, mothers dramatically increased their infant carrying behavior in families in which fathers were absent. Older siblings cared for infants more than did younger siblings, and brothers retrieved and carried infants more than did sisters. Individual expression of infant care changed to accommodate infant needs and changed according to varying social dynamics and circumstances across litters. Am. J. Primatol. 72:296–306, 2010. © 2009 Wiley‐Liss, Inc.     

Life history traits and parental care in Lepilemur ruficaudatus

In this study we investigated the importance of biparental care for the evolution and/or maintenance of pair-living in red-tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal folivorous lemur. Between 2000 and 2005, we collected data on life history traits from a total of 14 radio-collared pairs of adults and their offspring in Kirindy forest, western Madagascar. Predation rate varied between years with a minimum of 0% and a maximum of 40% per year. Patterns of parental care were quantified during simultaneous focal observations of both pair-partners in 2003 and 2004. Mating activity was limited to the months of May and June, as indicated by conspicuous changes of vulval morphology and male mate guarding behavior. After a gestation length of about 5 months, which is much longer than expected for a lemur of this body mass, single infants were born in November. Lactation lasted for about 50 days. Apart from lactation, females provided infant care by warming, grooming and transporting infants orally. Infants were parked in dense vegetation while females foraged. Males were seen only rarely in proximity to infants and we found no evidence for direct infant care provided by social fathers. We conclude that the necessity of direct infant care cannot explain the evolution and/or maintenance of pair-living in Lepilemur ruficaudatus.     

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.     

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.     

The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.