Father's Absence in the Mongolian gerbil (Meriones unguiculatus) is associated with alterations in paternal behavior, T, cort, presence of ERα, and AR in mPOA/ BNST.

Testosterone (T), estrogen receptor alpha (ERα), and androgen receptor (AR) play a significant role in the regulation of paternal behavior. We determined the effects of deprivation of paternal care on alterations in paternal behavior, T concentrations in plasma, and the presence of ERα and AR in the medial preoptic area (mPOA), bed nucleus of the stria terminalis (BNST), medial amygdala (MeA), and olfactory bulb (OB), as well as the corticosterone (CORT) concentrations in plasma caused by deprivation of paternal care in the Mongolian gerbil (Meriones unguiculatus). Twenty pairs of gerbils were formed; the pups were deprived of paternal care (DPC) in 10 pairs. In another 10 pairs, the pups received paternal care (PC). Ten males raised in DPC condition and 10 males raised in PC conditions were mated with virgin females. When they became fathers, each DPC male and PC male was subjected to tests of paternal behavior on day three postpartum. Blood samples were obtained to quantify T and CORT concentrations, and the brains were removed for ERα and AR immunohistochemistry analyses. DPC males gave less care to their pups than PC males, and they had significantly lower T concentrations and levels of ERα and AR in the mPOA and BNST than PC males. DPC males also had higher CORT concentrations than PC males. These results suggest that in the Mongolian gerbil father's absence causes a decrease in paternal care in the offspring, which is associated with alterations in the neuroendocrine mechanisms that regulate it.

Estudio piloto: contacto padre-hijo(a) y oxitocina en varones preparados especialmente para el nacimiento / Pilot study: father-child contact and oxytocin in males with a special education for childbirth

INTRODUCCÍON: Los padres se han involucrado cada vez más en el embarazo y el nacimiento de sus hijos, pero aún se requieren intervenciones paternas que permitan reubicar al padre en su rol de corresponsabilidad en la crianza. OBJETIVO: Observar el comportamiento-actitud paterna hacia el/la hijo(a) y la cantidad de oxitocina (OT) secretada en el nacimiento, en padres preparados de un modo especial para el parto. Método: Estudio piloto de 8 meses, parte de una investigación mayor cuali-cuantitativa de dos fases. La fase cualitativa inicial desarrolló una intervención preparatoria de padres para el nacimiento, con énfasis en la vinculación padre-hijo(a). La fase cuantitativa correspondió al piloto de la intervención paterna antenatal. RESULTADOS: Los padres presenciaron activamente el momento del expulsivo y el encuentro madre-hijo(a). Posteriormente, todos optaron por el contacto físico piel-piel con su hijo(a). La OT paterna experimentó un aumento (no significativo) durante el contacto padre-hijo(a) en comparación con la OT basal (momento inmediato al nacimiento). CONCLUSIONES: Padres preparados, sensibilizados y vinculados con su hijo(a) desde el embarazo experimentarían variaciones de la cantidad de OT cuando realizan contacto piel-piel con su hijo(a) en el nacimiento. Se requiere investigación experimental con una muestra mayor de participantes para concluir de manera categórica.

INTRODUCTION: Fathers have been increasingly involved in the pregnancy and birth of their children, but paternal interventions are still required to relocate the father in his role of co-responsibility in parenting. OBJECTIVE: To observe the paternal behavior-attitude towards the child and the amount of oxytocin (OT) secreted at birth in parents prepared (in a special way) for childbirth. METHOD: Pilot study of 8 months, part of a larger qualitative-quantitative research of two phases. The initial qualitative phase developed a male preparatory intervention for the birth, with emphasis on the father-child bonding. The quantitative phase corresponded to the pilot of the antenatal paternal intervention. RESULTS: Fathers actively witnessed the moment of delivery and the mother-child attachment. Subsequently, all of them opted for physical skin-to-skin contact with their child. Paternal OT experienced a (non-significant) increase during father-child contact, compared to baseline OT (immediately after birth). CONCLUSIONS: Males prepared, sensitized and involved with their child since pregnancy would experience variations in the amount of OT when they make father-child skin-to-skin contact at childbirth. Experimental research with a larger sample of participants is required to categorically reach a conclusion.

Motivational increase of androgens and behavior by infant distress calls in highly responsive common marmoset fathers, Callithrix jacchus.

Common marmoset fathers are highly involved in care of their infants. However, variability exists in their response to infant behavior even in paternally experienced fathers. Using infant distress cries as a motivation test, we investigated: 1. the differences in paternally experienced fathers' motivation to search for the infant vocalization stimuli; 2. the relationship between a father's motivation to search for the source of the infant cries and testosterone levels; and 3. if there is a rapid steroidogenesis pathway leading to increased testosterone and estradiol in the peripheral circulation. Only 44% of the paternally experienced fathers showed a high frequency of searching for the source of the infant distress cries. Through the use of multisteroid analysis, we found high responsive fathers had significantly higher levels of progesterone and testosterone in response to infant distress cries compared to a control stimulus with progesterone and androstenedione correlating with testosterone, while no differences were seen in low responders. The frequency to search for the infant stimuli was positively correlated with higher testosterone compared to control vocal levels. These results suggest that searching for the source of infant cries represents a motivation behavior for fathers that is activated by testosterone and reflects rapid circulating testosterone.

Uncovering the Sex-Specific Endocrine Responses to Reproduction and Parental Care.

Hormones mediate physiological and behavioral changes in adults as they transition into reproduction. In this study, we characterize the circulating levels of five key hormones involved in reproduction in rock doves (Columba livia): corticosterone, progesterone, estradiol, testosterone, and prolactin using univariate and multivariate approaches. We show similar patterns as previous studies in the overall patterns in circulating levels of these hormones, i.e., testosterone (males) and estradiol (females) high during nest-building or egg-laying, prolactin increasing at mid-incubation and peaking at hatching (both sexes), and elevated corticosterone levels in later incubation and early nestling development. In our investigation of hormone co-variation, we find a strong correlation between prolactin and corticosterone across sampling stages and similarities in earlier (early to mid-incubation) compared to later (late incubation to nestling d9) sampling stages in males and females. Finally, we utilized experimental manipulations to simulate nest loss or altered caregiving lengths to test whether external cues, internal timing, or a combination of these factors contributed most to hormone variation. Following nest loss, we found that both males and females responded to the external cue. Males generally responded quickly following nest loss by increasing circulating testosterone, but this response was muted when nest loss occurred early in reproduction. Similar treatment type, e.g., removal of eggs, clustered similarly in hormone space. These results suggest internal drivers limited male response early in reproduction to nest loss. In contrast, circulating levels of these hormones in females either did not change or decreased following nest manipulation suggesting responsiveness to external drivers, but unlike males, this result suggests that reproductive processes were decreasing.

Paternal and infanticidal behavior in the Mongolian gerbil (Meriones unguiculatus): An approach to neuroendocrine regulation.

This study aimed to provide evidence on estrogen and androgen pathways regulating the Mongolian gerbil's paternal and infanticidal behaviors (Meriones unguiculatus). We analyzed estrogen receptor alpha (ERα) and androgen receptor (AR) distribution in the medial preoptic area (mPOA), the bed nucleus of stria terminalis (BNST), as well as the anterior hypothalamic nucleus (AHN), the ventromedial hypothalamus nucleus (VMH), and the periaqueductal gray area (PAG) nuclei activated when males interact paternally or aggressively with the pups, respectively. Twenty aggressive males towards the pups and 10 paternal were selected through a screen paternal behavior test. Three groups of 10 males each were formed: paternal males (PAT), males with testosterone (T)-induced paternal behavior (T-PAT), and aggressive males (AGG). Male gerbils could interact with a pup for a few minutes, and their brains were removed and dissected for ERα and AR immunoreactivity (ir). The results showed that in T-PAT and PAT males, the number of ERα-ir and AR-ir cells in the mPOA/BNST was significantly higher than in AGG males. In AGG males, the number of ERα-ir and AR-ir cells in the AHN/VMH/PAG was significantly higher than PAT and T-PAT males. This difference in the presence of ERα and AR in nuclei activated in paternal interactions in the Mongolian gerbil supports the idea that these receptors participate in regulating paternal behavior. Also, these results suggest, for the first time, that they could be involved in the infanticidal behavior in this rodent.

Prefrontal cortex is associated with the rapid onset of parental behavior in inexperienced adult mice (C57BL/6).

There is significant variability in the immediate behavioral response displayed by inexperienced adult mice when exposed to pups for the first time. The aim of this study was to determine which brain regions were engaged (higher c-Fos-immunoreactivity, c-Fos-ir) when virgin females, that were exposed to pups for 15 or 60 min, displayed full parental behavior (FPB), partial parental behavior (PPB), or non-parental behavior (NPB), or virgin males displayed PPB or infanticidal behavior (IB). The number of c-Fos-ir neurons in the prelimbic cortex (PL) was higher in parental females than in the NPB group (after a 15-min exposure), and the group not exposed to pups (NE). C-Fos expression in the nucleus accumbens (NA) was increased in most groups of females exposed to pups compared to NE. Higher c-Fos-ir was also found in the shell subregion of the NA in infanticidal males, compared to males NE. The cortical (CoA) and medial (MA) amygdala also showed higher c-Fos-ir in parental females compared to NE animals. However, PPB and IB male groups also exhibited higher c-Fos-ir in the CoA and MA compared to the NE group. The expression of c-Fos in the different subregions of medial preoptic area and the ventromedial nucleus of the hypothalamus was not specifically associated with either parental or infanticidal behavior. No brain activation in males was specifically associated with infanticidal behavior. Our results suggest that 15 min of exposure to pups is enough to detect brain regions associated with parental behavior (PL) or pups processing (NA, MA, CoA) in mice. The PL might participate in the immediate onset of parental behavior in virgin females, coordinating and planning its rapid execution.

Preweaning Paternal Deprivation Impacts Parental Responses to Pups and Alters the Serum Oxytocin and Corticosterone Levels and Oxytocin Receptor, Vasopressin 1A Receptor, Oestrogen Receptor, Dopamine Type I Receptor, Dopamine Type II Receptor Levels in Relevant Brain Regions in Adult Mandarin Voles.

Although maternal separation and neonatal paternal deprivation (PD) have been found to exert a profound and persistent effects on the physiological and behavioural development of offspring, whether preweaning PD (PPD; from PND 10 to 21) affects maternal and parental responses to pups and the underlying neuroendocrine mechanism are under-investigated. Using monogamous mandarin voles (Microtus mandarinus), the present study found that PPD increased the latency to approach a pup-containing ball, decreased the total durations of sniffing and contacting a pup-containing ball and walking and increased the total duration of inactivity in both sexes. Moreover, PPD decreased serum oxytocin levels and increased corticosterone levels, but only in females. Furthermore, in both males and females, PPD decreased the expression of oxytocin receptor mRNA and protein in the medial preoptic area (MPOA), nucleus accumbens (NAcc) and medial prefrontal cortex (mPFC), but increased it in the medial amygdala (MeA) and decreased the expression of oestrogen receptor mRNA and protein in the MPOA. PPD increased the expression of dopamine type I receptor in the NAcc, but decreased it in the mPFC. PPD decreased dopamine type II receptor (D2R) in the NAcc both in males and females, but increased D2R in the mPFC in females and decreased D2R protein expression in males. Moreover, PPD decreased vasopressin 1A receptor (V1AR) in the MPOA, MeA and mPFC, but only in males. Our results suggest that the reduction of parental responses to pups induced by PPD may be associated with the sex-specific alteration of several neuroendocrine parameters in relevant brain regions.

Estradiol and estrogen receptor α in the mPOA and MeA in dwarf hamster (Phodopus campbelli) fathers.

E2 and its alpha receptor (ERα) have an essential role in the regulation of maternal behavior. In dwarf hamster (Phodopus campbelli), E2 facilitates the display of paternal care, and it is possible that ERα is part of the neuroendocrine mechanisms that regulate this behavior. The aim of this study was to analyze the influence of copulation, cohabitation with the pregnant mate and the presence of the pups on paternal behavior, circulating E2 levels and the presence of ERα in the medial preoptic area (mPOA) and medial amygdala (MeA) in dwarf hamsters. Eight males were mated with intact females (IFs), 8 with tubally ligated females (TLFs) and 8 with ovariectomized females (OFs). In males mated with IFs, paternal behavior tests were performed after copulation, halfway through pregnancy and 24 h after the birth of their pups. Males mated with TLFs were subjected to paternal behavior tests at equivalent periods as the males mated with IFs. In males mated with OFs, paternal behavior tests were performed on days 1, 5 and 10 of cohabitation. After the last paternal behavior tests, blood samples were taken for quantification of E2 by radioimmunoassay (RIA), and the brains were dissected to determine ERα immunoreactivity (ir) in the mPOA and MeA. Fathers mated with IFs had higher serum E2 concentrations and more ERα-ir cells in the mPOA than those of males mated with TLFs and OFs. These results suggest that E2 and its ERα may be associated with paternity in the dwarf hamster.

Consequences of placentophagia by adult virgin male California mice (Peromyscus californicus).

Placentophagia increases parental motivation in sexually inexperienced adult female rodents. We hypothesized that placenta ingestion has similar effects in virgin male California mice (Peromyscus californicus), a monogamous rodent in which fathers provide extensive care for their offspring. To test this hypothesis, we administered either a conspecific's placenta in oil or oil alone to adult virgin males via oral gavage. One, 7 or 24 hours later, each male underwent a 1-hour behavior test with either an unfamiliar pup or a novel object marble), immediately after which the mouse was perfused and the brain collected. Neural activation (Fos-immunoreactivity) was quantified in brain regions involved in parental care (bed nucleus of the stria terminalis, medial preoptic area, amygdala). We found few significant effects of placenta treatment, but at 7 h post-gavage, placenta-treated males had decreased latencies to approach both pups and marbles, compared to oil-treated controls (p = 0.05). Placenta-treated males also showed lower Fos-immunoreactivity in the dorsal bed nucleus of the stria terminalis, irrespective of stimulus type, compared to controls, both 1 h (p = 0.04) and 7 h (p = 0.05) post-treatment. These results suggest that placentophagia does not directly affect paternal motivation but might increase willingness to interact with novel stimuli in virgin male California mice.

Histone deacetylase inhibitor treatment promotes spontaneous caregiving behaviour in non-aggressive virgin male mice.

The majority of mammalian species are uniparental, with the mother solely providing care for young conspecifics, although fathering behaviours can emerge under certain circumstances. For example, a great deal of individual variation in response to young pups has been reported in multiple inbred strains of laboratory male mice. Furthermore, sexual experience and subsequent cohabitation with a female conspecific can induce caregiving responses in otherwise indifferent, fearful or aggressive males. Thus, a highly conserved parental neural circuit is likely present in both sexes; however, the extent to which infants are capable of activating this circuit may vary. In support of this idea, fearful or indifferent responses toward pups in female mice are linked to greater immediate early gene (IEG) expression in a fear/defensive circuit involving the anterior hypothalamus compared to that in an approach/attraction circuit involving the ventral tegmental area. However, experience with infants, particularly in combination with histone deacetylase inhibitor (HDACi) treatment, can reverse this pattern of pup-induced activation of fear/defence circuitry and promote approach behaviour. Thus, HDACi treatment may increase the transcription of primed/poised genes that play a role in the activation and selection of a maternal approach circuit in response to pup stimuli. In the present study, we investigated whether HDACi treatment would impact behavioural response selection and associated IEG expression changes in virgin male mice that are capable of ignoring, attacking or caring for pups. The results obtained indicate that systemic HDACi treatment induces spontaneous caregiving behaviour in non-aggressive male mice and alters the pattern of pup-induced IEG expression across a fear/defensive neural circuit.

Pattern of fos activation in the ventral tegmental area (VTA) of male prairie vole's (Microtus ochrogaster) in response to infant-related stimuli.

Prairie voles are socially monogamous mammals that form pair bonds and display paternal care. This study was focused on the male prairie vole's neuronal responses to infant-related odors. Using the fos protein as a measure of neuronal activation, we examined the brain responses of males to infant-related odors. Prior to testing, the subjects had cohabited for two weeks with either a male sibling (Male-Cohabited) or an unrelated female (Female-Cohabited). Given that paternal behavior of male prairie voles is enhanced after two-weeks of cohabitation with a mate, we hypothesized that fos activation in brain regions involved in caring must be increased in response to infants or their odors but not in response to water or sub-adult odors. To test this hypothesis, we analyzed the pattern of fos expression in the ventral tegmental area (VTA) and the bed nucleus of the stria terminals (BNST) two hours after Male-Cohabited and Female-Cohabited males were exposed to either two live infants or to odors of infants, sub-adults or water. Results showed differences in fos expression within the VTA between Male-Cohabited and Female-Cohabited subjects that were exposed to infants and infant odors. The type of cohabitation had no effect on fos expression within the BNST, but the pattern of fos activation in this region differed by the type of odor to which the subjects were exposed. Together, the data indicate that female sensory cues during post-mating cohabitation may be processed within the VTA to direct the male prairie vole's responses towards infants.

Paternal behavior in the Mongolian gerbil, and its regulation by social factors, T, ERα, and AR.

The present study evaluates the role of social factors in the transition from infanticidal to paternal male behavior and its association with T concentration, presence of estrogen receptor alpha (ERα) and androgen receptor (AR) in the olfactory bulb (OB), medial preoptic area (mPOA) and medial amygdala (MeA) of Mongolian gerbils (Meriones unguiculatus). This study included thirty-six sexually inexperienced males displaying aggressive behavior toward foreign pups. The selected animals were mated and organized into four groups. The paternal behavior tests were performed on the day of copulation (DCOPUL), during cohabitation with a pregnant female (CPREG), on the day of birth (DBIRTH), and on day 6 postpartum (DPP6). Eight sexually inexperienced males (CTL (male-male cohabitation) were used as control. After paternal behavior tests, blood samples were obtained to quantify T by radioimmunoassay; the brains were removed and analyzed for immunoreactivity (ir) of ERα and AR. All males of the DCOPUL, DBIRTH, and DPP6 groups exhibited paternal behavior, whereas the males of CPREG and CTL groups were aggressive with the pups. Paternal behavior was associated with high T concentrations, and the presence of ERα-ir and AR-ir in the OB, MeA, and mPOA. These results suggest that the transition from aggressive to paternal response to pups is facilitated by copulation, and that in this transition is involved an increase in T concentration. Moreover, the presence of ERα-ir and AR-ir in the OB, mPOA, and MeA could indicate that estrogenic and androgenic pathways participate in the regulation of paternal behavior of the Mongolian gerbils.

Neuronal activation associated with paternal and aversive interactions toward pups in the Mongolian gerbils (Meriones unguiculatus).

Approach/avoid model is used to analyze the neural regulation of maternal behavior in the laboratory rat. This model proposes that the medial preoptic area (mPOA) and bed nucleus of stria terminalis (BNST) are brain regions involved in facilitating mechanisms. By contrast, anterior hypothalamic nucleus (AHN), ventromedial hypothalamic nucleus (VMH), and periaqueductal gray participate in the inhibiting mechanisms of neural regulation of maternal behavior. We hypothesized that there are also facilitating and inhibiting mechanisms in the neural regulation of paternal behavior. Here, we determined which neural areas are activated during paternal and aversive interactions with pups in the Mongolian gerbils (Meriones unguiculatus). By testing paternal behavior, we selected 40 males aggressive toward pups and 20 paternal males. These males were organized into six groups of 10 animals in each group: aggressive males that interacted with pups (AGG-pups) or candy (AGG-candy), paternal males that interacted with pups (PAT-pups) or candy (PAT-candy), and males with testosterone (T)-induced paternal behavior that interacted with pups (IPAT-pups) or candy (IPAT-candy). After interacting with pups or candy, the brains were extracted and analyzed for immunoreactivity (ir) with c-fos. Males that interacted with pups had significantly higher c-fos-ir in the mPOA/BNST than males that interacted with candy. Males that displayed aggression had significantly higher c-fos-ir in the AHN, VMH, and periaqueductal gray than aggressive males that interacted with candy. These results suggest that in the neural regulation of paternal behavior in the Mongolian gerbil underlie positive and negative mechanisms as occurs in maternal behavior.

Dynamic regulation of brain aromatase and isotocin receptor gene expression depends on parenting status.

Fathering behavior is critical for offspring survival in many species across diverse taxa, but our understanding of the neuroendocrine mechanisms regulating paternal care is limited in part because of the few primarily paternal species among the common animal models. However, many teleosts display primarily paternal care, and among the teleosts, anemonefish species are particularly well suited for isolating molecular mechanisms of fathering as they perform parental care in isolation of many other typically competing behaviors such as territorial defense and nest building. The goal of this study was to determine the extent to which whole brain gene expression levels of isotocin receptors, arginine vasotocin receptors, and aromatase as well as circulating levels of the bioactive sex steroid hormones estradiol (E2) and 11-ketotestosterone (11KT) vary in association with parenting behavior in Amphiprion ocellaris. Brain aromatase and IT receptor gene expression were higher in both males and females that were parenting versus not. IT receptor expression was overall higher in males than females, which we interpret is a reflection of the greater parental effort that males display. Aromatase was overall higher in females than males, which we conclude is related to the higher circulating E2, which crosses into the brain and increases aromatase transcription. Results suggest both aromatase and IT receptors are dynamically upregulated in the brains of A. ocellaris males and females to support high levels of parental effort.

Inhibiting ERα expression in the medial amygdala increases prosocial behavior in male meadow voles (Microtus pennsylvanicus).

This study tested the hypothesis that site-specific estrogen receptor alpha (ERα) expression is a critical factor in the expression of male prosocial behavior and aggression. Previous studies have shown that in the socially monogamous prairie vole (Microtus ochrogaster) low levels of ERα expression, in the medial amygdala (MeA), play an essential role in the expression of high levels of male prosocial behavior and that increasing ERα expression reduced male prosocial behavior. We used an shRNA adeno-associated viral vector to knock down/inhibit ERα in the MeA of the polygynous male meadow vole (M. pennsylvanicus), which displays significantly higher levels of ERα in the MeA than its monogamous relative. Control males were transfected with a luciferase expressing AAV vector. After treatment males participated in three social behavior tests, a same-sex dyadic encounter, an opposite-sex social preference test and an alloparental test. We predicted that decreasing MeA ERα would increase male meadow vole's prosocial behavior and reduce aggression. The results generally supported the hypothesis. Specifically, MeA knockdown males displayed lower levels of defensive aggression during dyadic encounters and increased levels of overall side-x-side physical contact with females during the social preference test, eliminating the partner preference observed in controls. There was no effect on pup interactions, with both treatments expressing low levels of alloparental behavior. Behaviors affected were similar to those in male prairie voles with increased ERα in the BST rather than the MeA, suggesting that relative changes of expression within these nuclei may play a critical role in regulating prosocial behavior.

The neoteny-helper hypothesis: When to expect and when not to expect endocrine mechanisms to regulate allo-parental care?

Family groups with helpers occur in several species of fish, birds and mammals. In such cooperatively breeding species all group members help with raising the offspring, i.e. parents and offspring from previous litters. While the ecological reasons and ultimate consequences of allo-parental care have been studied in detail, we know little about its physiological regulation. We propose three alternative hypotheses for the endocrine regulation of allo-parental care. 1. The neoteny-helper hypothesis predicts that helpers that did not undergo adolescence yet show helping behavior without any endocrine mechanisms activating it, as helping is the default response towards infant stimuli. The endocrine changes during adolescence would then deactivate helping behavior. 2. The parent-helper hypothesis predicts that helpers undergo the same endocrine changes as parents (increased prolactin and corticosterone levels; decreased testosterone in males but increased estrogen in females). We predict that this hypothesis is especially important in post-adolescent helpers. 3. The helper-specific hypothesis predicts that there are specific endocrine mechanisms that only exist in helpers but not in breeders. We review evidence for these three hypotheses in 23 species of fish, birds, and mammals. We found no evidence for the helper-specific hypothesis but for both other hypotheses. As predicted, this depended on whether helpers were pre- or post-adolescent, but information on whether or not helpers underwent adolescence was often missing. Thus, future studies should investigate whether or not helpers have reached sexual maturity, differentiate between pre- and post-adolescent helpers, and study behavioral changes in helping behavior during adolescence. We conclude that the neurobiological circuits in the brain necessary for allo-parental care might often be the default stage in helpers from cooperative breeding species, which might be deactivated by specific endocrine mechanisms during adolescence, and then would need reactivation for allo-parental and parental care.

Physiological mechanisms mediating patterns of reproductive suppression and alloparental care in cooperatively breeding carnivores.

Although cooperation represents a long-standing evolutionary puzzle, field studies on social carnivores have contributed greatly to our understanding of the selective forces favoring cooperative breeding. Despite these insights, our grasp of the proximate mechanisms facilitating cooperation in carnivores remains surprisingly limited. Here we provide an overview of our current knowledge of the endocrine mechanisms mediating cooperative breeding in terrestrial species belonging to the mammalian order Carnivora. We focus primarily on aspects of reproductive suppression and alloparental care. We find few studies on the topic, with some of the best studies focusing on the behavioral endocrinology of cooperative breeding in canids (dogs) and herpestids (mongooses). Overall, these studies suggest that breeding females typically have higher circulating levels of estrogen, luteinizing hormone, progesterone, and prolactin than do non-breeding adult females. We also find that among males, testosterone levels are often elevated in breeders compared to non-breeding adult males. The effect of glucocorticoids on reproductive suppression in carnivores appears to be sex-specific: breeding males typically have higher glucocorticoid levels than their non-breeding subordinates, but there is no clear pattern for breeding females. Finally, elevated levels of prolactin and oxytocin are consistently associated with alloparental care in cooperatively breeding carnivores, whereas testosterone and glucocorticoids are often lower in individuals who participate in alloparenting. Taken together, our synthesis elucidates striking gaps in our knowledge of carnivore physiology, especially the endocrine mechanisms promoting alloparental care, and we identify important areas for future research.

Factors that influence the onset of parental care in zebra finches: Roles for egg stimuli and prolactin.

Parental care is a critical component for determining reproductive success both for a current set of offspring but also over the lifetime of the individual. The hormone prolactin has often been implicated as a parental care hormone across taxa but causal relationships have only been strongly demonstrated in mammals and in a few select species of birds. For instance, in mammals, maternal care towards foster pups can be induced by exogenous treatment with prolactin, in concert with other reproductive hormones involved in pregnancy. We aimed to address this causal mechanism in birds by artificially elevating prolactin during the nest building and egg laying stages using vasoactive intestinal peptide (VIP) and then exposing them to foster chicks. We predicted that increasing prolactin would increase brooding and feeding behaviors towards foster chicks compared to the saline control group. Parental behavior towards foster chicks was only shown by individuals who had initiated clutches regardless of treatment. VIP treatment had no effect on parental behavior; however, a positive relationship was found between male and female feeding rates in the VIP but not control group. Our results suggest that both eggs and chicks are sufficient to stimulate foster care, perhaps through endogenous prolactin signalling, while further elevations of prolactin may serve to synchronize parental behaviors between pairs.

Different behavioral, neural and neuropeptide responses of fathers to their own and to alien pups in mandarin voles.

Mothers often prefer to care for their own offspring rather than those of other females. However, whether fathers respond differently to their own pups and to alien ones remains unclear. In this study, we found that male mandarin voles (Microtus mandarinus) directed more sniffing toward their own pups than toward alien pups. The numbers of Fos-immunoreactive neurons in the medial preoptic nucleus, bed nucleus of the stria terminalis, nucleus accumbens, anterior cingulate cortex were significantly increased when fathers were exposed to an alien pups; however, more brain regions such as paraventricular nucleus, hypothalamic supraoptic nucleus, lateral habenula, ventral lateral septal nucleus, and medial amygdaloid nucleus showed increased number of Fos-immunoreactive neurons activated when the fathers were exposed to their own pups. Exposure to their own pups also induced a greater number of Fos-immunoreactive neurons in the anterior cingulate cortex, paraventricular nucleus, hypothalamic supraoptic nucleus, lateral habenula, ventral lateral septal nucleus and medial amygdaloid nucleus, as well as higher expression of oxytocin and vasopressin in the paraventricular nucleus, compared with exposure to alien pups. Our results indicated that fathers demonstrated different behavioral and neural responses to their own and to alien pups.

Estrogen-dependent modifications to hippocampal plasticity in paternal California mice (Peromyscus californicus).

In many biparental species, mothers and fathers experience similar modifications to circulating hormones. With these modifications come alterations in neural structure and function suggesting that neuroendocrine mechanisms may underlie postpartum plasticity in both males and females. In the biparental California mouse (Peromyscus californicus), adult neurogenesis is maintained and anxiety-like behavior is attenuated in fathers during the mid-postpartum period. Given a causal relationship between estrogen and regulation of both adult neurogenesis and anxiety, we aimed to elucidate the role of estrogen-dependent mechanisms in paternal experience-related modifications to hippocampal neuroplasticity in California mice. In Experiment 1, hippocampal estrogen receptor beta (ERß) mRNA expression, along with circulating estradiol concentrations, were determined throughout the postpartum period. An upregulation in ERß expression was observed in postnatal day 16 males compared to virgins. Additionally, a rise in circulating estradiol concentrations was detected on postnatal day 2 compared to virgins; levels began to decline toward virgin levels on postnatal day 16 and postnatal day 30. In Experiment 2, we determined the role of estrogen-dependent mechanisms in adult neurogenesis and anxiety-like behavior by treating virgin and paternal males with saline or the selective estrogen receptor modulator, tamoxifen (TMX), during the time of axon extension (i.e., one week after bromodeoxyuridine injection). While TMX failed to alter elevated plus maze performance, TMX treatment inhibited survival of adult born neurons but only in paternal mice. These findings highlight the potential for estrogen-dependent pathways to mediate hippocampal adult neurogenesis in paternal mice.