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Maternal behavior, paternal behavior, and pup survival in CD-1 albino mice (Mus musculus) in three different housing conditions.

Parental behavior, food consumption, and pup development in litters of CD-1 albino mice (Mus musculus) with single mothers or paired mothers in 3 different housing conditions were compared. Fewer pups survived when parents were required to run in a wheel to obtain food, and these pups had lower weights than pups in the wheel-noncontingent and no-wheel groups. The presence of the male facilitated pup survival in the wheel-contingent group but had no effect on pup growth. Mice in the wheel-contingent group ran more revolutions than those in the wheel-noncontingent group and spent less time in parental care. In the wheel-contingent group, males spent more time running and ate less food than females, suggesting that males may indirectly facilitate pup development by providing food for the mother. The results suggest that the presence of the male increases pup care and may facilitate maternal behavior under appropriate environmental conditions.

Animals↗

Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior.

The effects of aromatase within the brain on sexual behavior have been studied in a wide variety of species. Relatively few non-mating behaviors have been considered, despite evidence that estrogen affects many social behaviors. Testosterone promotes paternal behavior in California mouse (Peromyscus californicus) fathers, acting primarily via aromatization to estradiol. Virgin male California mice rarely exhibit paternal behavior, so we investigated whether aromatase in the brain changed with the onset of paternal behavior in California mouse fathers. In the medial preoptic area (MPOA), a brain area known to regulate parental behavior in rodents, we found that fathers had significantly more aromatase activity than mated males without pups, suggesting that an increase in estrogen production in this brain area contributes to the onset of paternal behavior. We also found that progesterone (P(4)) levels were lower in fathers compared to sexually inexperienced males and that P(4) was negatively correlated with aromatase activity in the MPOA. These P(4) findings agree with a recent study that found an inhibitory effect of P(4) on paternal behavior. Overall, we found that aromatase activity and P(4) levels change in association with an important life history transition, and may provide a mechanistic basis for plasticity in paternal behavior.

Animals↗

Central vasopressin administration regulates the onset of facultative paternal behavior in microtus pennsylvanicus (meadow voles).

Pharmacological experiments have implicated a role for central arginine vasopressin (AVP) in regulating paternal behavior in monogamous prairie voles. Although nonmonogamous meadow voles exhibit appreciable paternal care when housed under winter, short day lengths (SD), no research has examined whether the same neurobiological systems are involved in regulating paternal behavior in a nonmonogamous species when it behaves paternally. The goal of these experiments was to determine whether central administration of AVP, but not cerebrospinal fluid (CSF), affected the suppression of pup-directed aggression and/or the onset of paternal behavior in meadow voles. Data from experiment 1 implicated a role for AVP in facilitating changes in male behavior: central administration of 1 ng of AVP (but not 3 ng or CSF) inhibited pup-directed aggression in previously pup-aggressive males, and 3 ng of AVP (but not 1 ng or CSF) induced paternal behavior in previously nonpaternal males. In contrast, AVP (1 and 3 ng) did not enhance paternal behavior in already paternal males. Experiment 2 tested the specificity of AVP. Previous research indicated that 24 h of unmated cohabitation with a female reliably induced paternal behavior in SD males. Hence, experiment 2 examined whether administration of a V(1a) AVP antagonist (AVPA), but not CSF, prior to 24 h of unmated cohabitation would block the onset of paternal behavior. Males that received CSF displayed paternal behavior faster and engaged in more investigatory and paternal behaviors than males that received AVPA. Thus, pharmacological experiments support the hypothesis that AVP likely regulates paternal behavior in both facultatively and consistently paternal vole species.

Aggression↗

Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus).

Testosterone (T) mediates a trade-off, or negative correlation, between paternal behavior and aggression in several seasonally breeding avian species. However, the presence or absence of a T-mediated trade-off in mammals has received less attention. We examined the relationship between paternal behavior and territorial aggression in the biparental California mouse, Peromyscus californicus. In contrast to seasonally breeding birds, T maintains paternal behavior in this year-round territorial species. Castration reduced paternal behavior, whereas T replacement maintained high levels of paternal behavior. We hypothesize that T is aromatized in the brain to estradiol, which in turn stimulates paternal behavior. In contrast to paternal behavior, aggressive behavior was not reduced by castration. Interestingly, only sham males showed an increase in aggression across three aggression tests, while no change was detected in castrated or T-replacement males. Overall, trade-offs between aggression and paternal behavior do not appear to occur in this species. Measures of paternal behavior and aggression in a correlational experiment were actually positively correlated. Our data suggest that it may be worth reexamining the role that T plays in regulating mammalian paternal behavior.

Aggression↗

Limbic system fos expression associated with paternal behavior.

Axon-sparing lesions of the medial nucleus of the amygdala (MeA) decrease male parental behavior in the highly social prairie vole. To assess further the role of the amygdala in paternal behavior, male and female prairie voles were exposed to a pup or a non-social olfactory stimulus for 3 hours, and cells expressing Fos peptide were labelled using immunocytochemistry. Compared to controls, males exposed to a pup showed an increase in Fos expression in the MeA, as well as in several areas with connections to it: the accessory olfactory bulb, lateral septum, medial preoptic area, medial bed nucleus of the stria terminalis, nucleus reuniens and paraventricular nucleus of the thalamus. There was no increase in Fos immunoreactivity in the paraventricular nucleus of the hypothalamus or piriform cortex. The same pattern of Fos expression was found in female voles, with the exception of the thalamic paraventricular nucleus, where there was an increase in the pup-exposed group that was not statistically significant (P = 0.11). In addition, the magnitude of induction in females was markedly less than that in males in the medial preoptic area. These results provide further evidence that the MeA is involved in paternal behavior, and suggest certain other areas previously implicated in meternal behavior may also be involved in the control of paternal behavior in this species.

Animals↗

Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors.

Several lines of evidence have implicated the neurohypophyseal peptide, vasopressin (VP), in the mediation of complex social behaviors including affiliation, aggression, juvenile recognition and parental behavior. Recent studies in microtine rodents using cellular, molecular and behavioral approaches provide additional evidence suggesting a role for VP in the formation of pair bonding and male parental care. Monogamous and promiscuous voles differ in social behaviors such as mating-induced pair bonding, selective aggression, and male parental care. Comparative studies have demonstrated that they also differ in dynamics of VP synthesis and release associated with reproduction, in the distribution pattern and regional quantity of VP receptors, and in the promoter sequence of the V1a receptor gene. In monogamous prairie voles, (Microtus ochrogaster), brain administration of VP induces pair bonding and male parental care whereas administration of the VP antagonist diminishes these behaviors. Together, these data suggest that VP is involved in the regulation of social behaviors in monogamous voles and differences in the brain VP system may underlie species differences in behavior and life strategy in voles.

Animals↗

Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice.

The role of arginine vasopressin (AVP) in the nongenomic transfer of paternal behavior from fathers to offspring was examined in Peromyscus. Male California mice (P. californicus) exposed to fewer retrievals by white-footed mouse (P. leucopus) foster parents displayed fewer retrievals of biological offspring. In contrast, white-footed mice were retrieved equally rarely by California mouse foster parents and by biological parents and displayed no changes in pup retrieval behavior. AVP-immunoreactive staining in the bed nucleus of the stria terminalis may predict paternal behavior because it correlated positively with retrievals and with a score consisting of huddling, grooming, and time inside the nest. The authors discuss AVP as a possible mechanism by which early experience shapes adult paternal behavior.

Animals↗

Social and environmental factors influence the suppression of pup-directed aggression and development of paternal behavior in captive meadow voles (Microtus pennsylvanicus).

During summer, female meadow voles (Microtus pennsylvanicus) maintain territories and males do not engage in paternal care. As day length shortens, territories dissolve and males nest with females and young. Because paternal behavior has never been studied in free-living meadow voles during colder months or in the laboratory under short photoperiods, the authors examined whether males housed in short day (SD) lengths exhibited more frequent or better quality paternal behavior than males housed in long day (LD) lengths. Sexually and parentally inexperienced (naive) SD males exhibited proportionally more and qualitatively better paternal care than naive LD males. SD males were more responsive than LD males to classic social cues associated with prepartum aggression inhibition and paternal onset. SD sires also displayed qualitatively better paternal behavior than LD sires. These data suggest that meadow vole paternal state is regulated by specific social and environmental cues that may contain reliable information about ecological conditions that favor paternal care.

Aggression↗

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.

Animals↗

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.

Animals↗

Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster).

The density of vasopressin-immunoreactive (AVP-ir) fibers in the lateral septum and lateral habenular nucleus is lower in prairie vole fathers--which display paternal behavior under natural conditions-than in sexually naive males. To see if these changes occur before or after the birth of pups, and whether they are related to changes in paternal behavior, we tested paternal responsiveness and measured AVP-ir fiber density in the lateral septum, lateral habenular nucleus, medial preoptic area, and paraventricular nucleus of the thalamus of sexually naive males and females (0P) and breeding pairs that were sacrificed shortly after mating (3P); during early (13P); or late gestation (21P); or after the birth of pups (6PP). Paternal responsiveness was increased in 3P males and reached a plateau in 13P males. AVP-ir fiber density did not change in the medial preoptic area and the paraventricular nucleus of the thalamus. The fiber density in the lateral septum and lateral habenular nucleus was affected differently in males and females. Among males, 3P animals had the lowest fiber density, while 13P and 6PP animals had an intermediate, and 0P and 21P animals the highest fiber density, whereas among females, no differences in fiber density were found. A second experiment showed that the decrease in fiber density in 3P males could be induced by cohabitation with an unfamiliar female but not by an unfamiliar male nor by relocation to a novel cage. The changes in AVP-ir fiber density shortly after mating suggest that these fibers may be involved in paternal responsiveness as well as in various other social behaviors that change after mating.

Amygdala↗

Paternal behavior in the spiny mouse (Acomys cahirinus).

The responsiveness of adult male spiny mice (Acomys cahirinus) to both their own and alien precocial young was investigated. Paternal behavior was manifested primarily by the males huddling with their offspring and the coordination of pup attendance between adult males and females. With less than 2 days exposure to their own neonates, males were found to discriminate between their own and alien young. Experience plays an important role in the development of paternal behavior in spiny mice. Males who have never had pups of their own sniff and attack unfamiliar neonates more than males who have fathered pups. The adaptive significance of paternal investment in this uniquely precocial murid rodent was discussed.

Adaptation, Biological↗

Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster).

Castration reduced paternal responsiveness of male prairie voles (Microtus ochrogaster). Castration also reduced the number of vasopressin immunoreactive (AVP-ir) cells in the bed nucleus of the stria terminalis (BST) and medial amygdaloid nucleus (MA), as well as the density of AVP-ir fibers in the lateral septum. Testosterone treatment of castrated voles prevented these changes. The similarities in the effects of the hormonal manipulations on paternal responsiveness and AVP immunoreactivity provide further support for the hypothesis that AVP-ir projections of the BST and MA are implicated in paternal behavior.

Amygdala↗

Elevated 11-ketotestosterone during paternal behavior in the Bluebanded goby (Lythrypnus dalli).

The relationship between androgens and paternal behavior is not straightforward, potentially because of the diversity of tasks a male must undertake to maximize reproductive success, notably alternating between courtship, aggression, and offspring care. In some species, these events are separated in time, but in others they are coincident. The endocrine profiles of species that simultaneously court, parent, and defend a nest, such as male bluebanded gobies (Lythrypnus dalli), are not well understood. We sampled a potent fish androgen, 11-ketotestosterone (KT), at different life history stages (experienced parenting males, experienced males not actively parenting, inexperienced males with their first clutch, and females), to examine this relationship. We found that experienced parenting L. dalli males have the highest KT levels of any group, while none of the other groups differed significantly. Males showed elevated KT levels when they had eggs compared to when they did not. Our data suggest that KT facilitates at least some aspects of parental care in L. dalli.

Animals↗

Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli).

Biparental male hamsters, Phodopus campbelli, act as midwives during the birth of their litter and are highly responsive to an experimentally displaced pup. They also have high peripheral concentrations of estradiol, a hormone with known roles in maternal behavior. Surgical castration during the gestation of their first litter was used to investigate the source of that estradiol and the functional role of testicular sex steroids in paternal responsiveness. In Experiment I, castration reduced both testosterone and estradiol concentrations, confirming that the testes were the primary source of estradiol. However, neither paternal responsiveness nor multiple measures of reproductive success were altered by the castration. Aggression directed towards an intruder, however, was reduced by castration. In Experiment II, removal of prior experience with birth or pups also failed to alter paternal responsiveness in castrated males. Although the present results do not preclude a role for local estradiol synthesis in the brain, results do not support an association between high circulating estradiol in males and their paternal behavior.

Aggression↗

Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring.

Parental care has been demonstrated to have important effects on offspring behavioral development. California mice (Peromyscus californicus) are biparental, and correlational evidence suggests that pup retrieving by fathers has important effects on the development of aggressive behavior and extra-hypothalamic vasopressin systems. We tested whether retrievals affected these systems by manipulating paternal retrieval behavior between day 15 and 21 postpartum. Licking and grooming behavior affect behavioral development in rats, so we also experimentally reduced huddling and grooming behavior by castrating a subset of fathers. Experimentally increasing the frequency of paternal pup retrieving behavior decreased attack latency in resident-intruder in both male and female adult offspring, whereas experimental reduction of huddling and grooming had no effect. In a separate group of male offspring, we examined vasopressin immunoreactivity (AVP-ir) in two regions of the posterior bed nucleus of the stria terminalis (BNST): the dorsal fiber tracts (dBNST) and the ventral cell body-containing region (vBNST). Experimentally increasing retrievals led to an apparent shift in AVP-ir distribution. Specifically, offspring from the high retrieval group had more AVP-ir than offspring from the sham retrieval group in the dBNST, whereas the opposite was observed in the vBNST. Experimental reduction of paternal grooming was associated with increased AVP-ir in the paraventricular nucleus and also increased corticosterone and progesterone, similar to observed effects of maternal grooming on HPA function. This study provides further evidence that paternal behavior influences the development of aggression and associated neural substrates.

Aggression↗

Paternal behavior is associated with central neurohormone receptor binding patterns in meadow voles (Microtus pennsylvanicus).

Paternal and nonpaternal voles (microtus) have different arginine-vasopressin (AVP) and oxytocin (OT) receptor patterns in the extended amygdala, a neural pathway associated with parental behavior. Using receptor autoradiography, the authors examined whether AVP and OT receptor patterns were associated with facultative paternal behavior in either sexually and parentally inexperienced or experienced meadow voles (Microtus pennsylvanicus). Experienced, in contrast to inexperienced, males had less AVP binding in the lateral septum (LS), more AVP binding in the anterior olfactory nucleus (AON), and more OT binding in the AON, bed nucleus of the stria terminalis, LS, and lateral amygdala. Thus, specific AVP receptor patterns, which co-occur with paternal care in consistently paternal voles, also may be associated with paternal care (when present) in typically nonpaternal species. This study also demonstrated a possible relationship between OT receptor patterns and paternal state in male mammals.

Amygdala↗