Search

Costs of parental care can include increased physical, physiological, and behavioral demands and reduced prospects for future reproduction. Therefore, animals may benefit from recognizing and discriminating their own offspring during the period of infant care to ensure that they provide care only to their own young. Differences in offspring discrimination between mothers and fathers may arise due to differences in the amount of parental care they provide. In mammals, mothers bear the costs of gestation and lactation, while fathers do not; therefore, we might expect that in mammal species in which both parents provide parental care, mothers will show greater levels of offspring discrimination than fathers. In the present study, we examined possible sex differences in offspring discrimination in the biparental, monogamous California mouse (Peromyscus californicus) across the lactational period. On postpartum days (PPD) 3, 7, 16, and 28, parents were housed individually in a test cage and presented simultaneously with two wire mesh balls, one containing their own pup and the other containing an unrelated pup. On individual test days, parents behaved similarly toward the two balls. Fathers, but not mothers, showed significant changes in latencies to approach and interact with the non-kin ball across test days, but no clear pattern was observed. Fathers also approached the non-kin ball more frequently than mothers when pups reached weaning age (PPD 28). Thus, fathers may show increased interest in unrelated young as their offspring become independent.

To investigate flexibility in vocal signaling by rodent pups, we examined whether olfactory stimuli influence characteristics of pup calls and how these calls may be affected by sex and litter size in California mice (Peromyscus californicus). Pups were isolated and recorded during a 3-min baseline period followed by a 5-min exposure to bedding containing scent from their home cage, scent from the home cage of an unfamiliar family, coyote urine, or no scent (control). Latency to call, call rate, and call characteristics (duration, frequency, and amplitude) were compared between the baseline and scent-exposure periods and among olfactory conditions. Compared with the control condition, pups from two-pup litters called more quietly when exposed to odor from a predator, whereas pups from three-pup litters called more loudly. Additionally, pups showed nonsignificant tendencies to reduce call rates in response to odors from their home cage and to increase call rates when exposed to predator urine. Last, males produced higher-frequency calls and more ultrasonic vocalizations than females. These results indicate that pup calling behavior in this species can be influenced by acute olfactory stimuli as well as litter size and sex. The flexibility of pup calling in response to these three variables potentially increases the communication value of pup calls and helps shape the parents' responses.

In biparental species, in which both parents care for their offspring, the neural and endocrine mediators of paternal behavior appear to overlap substantially with those underlying maternal behavior. Little is known, however, about the roles of classical neurotransmitters, such as norepinephrine (NE), in paternal care and whether they resemble those in maternal care. We tested the hypothesis that NE facilitates the initiation of nurturant behavior toward pups in virgin male and female California mice (Peromyscus californicus), a biparental rodent. Virtually all parents in this species are attracted to familiar and unfamiliar pups, while virgins either attack, avoid, or nurture pups, suggesting that the neurochemical control of pup-related behavior changes as mice transition into parenthood. We injected virgin males and females with nepicastat, a selective dopamine β-hydroxylase inhibitor that blocks NE synthesis (75 mg/kg, i.p.), or vehicle 2 h before exposing them to a novel pup, estrous female (males only), or pup-sized novel object for 60 min. Nepicastat significantly reduced the number of males and females that approached the pup and that displayed parental behavior. In contrast, nepicastat did not alter virgins' interactions with an estrous female or a novel object, suggesting that nepicastat-induced inhibition of interactions with pups was not mediated by changes in generalized neophobia, arousal, or activity. Nepicastat also significantly reduced NE levels in the amygdala and prefrontal cortex and increased the ratio of dopamine to NE in the hypothalamus. Our results suggest that NE may facilitate the initiation of parental behavior in male and female California mice.

In rodents, young pups communicate with their parents through harmonic calls and ultrasonic vocalizations (USVs). These forms of communication can improve chances of survival, since pups rely on their parents for thermoregulation, nutrition and protection. The extent to which pups modulate calls in response to their surroundings remains unclear. In this study we examined whether olfactory stimuli influence characteristics of pup calls, and how these calls may be affected by pup sex and litter size, in the California mouse (Peromyscus californicus). Pups were isolated and audio recorded during an initial, 3-minute control period, after which they were exposed for 5 minutes to bedding containing one of 4 olfactory cues: scent from their home cage, scent from the home cage of an unfamiliar family, coyote urine, or no scent. Latency to call, call rate, call duration and call characteristics (e.g. frequency and amplitude) were compared between the control period and olfactory-exposure period as well as among olfactory conditions. Pups from 2-pup litters called more quietly (lower amplitude) when exposed to odor from a predator while pups from 3-pup litters called louder (higher amplitude). Additionally, pups tended to reduce their call rates in response to odors from their home cage, consistent with contact quieting. However, pups tended to increase their rate of calling when exposed to predator urine, in contrast to the expectations of predator-induced vocal suppression. Lastly, male pups produced higher-frequency calls and more USVs than females. These results indicate that a number of pup call characteristics in this species can be influenced by acute olfactory stimuli as well as factors such as litter size and sex. The value of these pup call variations for offspring-parent communication is unclear: whether they elicit different parental responses is unknown and would be an interesting/valuable/informative avenue for future studies.

In male mammals that provide care for their offspring, fatherhood can lead to changes in behavioral, morphological, and physiological traits, some of which might constitute trade-offs. Howe...

Exercise behavior is under partial genetic control, but it is also affected by numerous environmental factors, potentially including early-life experiences whose effects persist into adulthood. We studied genetic and early-life environmental effects on wheel-running behavior in a mouse model that includes four replicate high runner (HR) lines selectively bred for increased voluntary wheel running as young adults and four non-selected control (C) lines. In a full factorial design, mice from each line were granted wheel access or not and administered either standard or Western diet (WD) from weaning (3 weeks old) to 6 weeks of age (sexual maturity). In addition to acute effects, after a washout period of 8 weeks (∼6 human years) in which all mice had standard diet and no wheel access, we found both beneficial and detrimental effects of these early-life exposures. During the first week of treatments, WD increased distance run by 29% in C mice and 48% in HR mice (significant Diet × Linetype interaction), but diet effects disappeared by the third week. Across the three weeks of juvenile treatment, WD significantly increased fat mass (with lean mass as a covariate). Tested as adults, early-life exercise increased wheel running of C mice but not HR mice in the first week. Early-life exercise also reduced adult anxiety-like behavior and increased adult fasted blood glucose levels, triceps surae mass, subdermal fat pad mass, and brain mass, but decreased heart ventricle mass. Using fat mass as a covariate, early-life exercise treatment increased adult leptin concentration. In contrast, early-life WD increased adult wheel running of HR mice but not C mice. Early-life WD also increased adult lean mass and adult preference for Western diet in all groups. Surprisingly, early-life treatment had no significant effect on adult body fat or maximal aerobic capacity (VO2max). No previous study has tested for combined or interactive effects of early-life WD and exercise. Our results demonstrate that both factors can have long-lasting effects on adult voluntary exercise and related phenotypes, and that these effects are modulated by genetic background. Overall, the long-lasting effects of early-life exercise were more pervasive than those of WD, suggesting critical opportunities for health intervention in childhood habits, as well as possible threats from modern challenges. These results may be relevant for understanding potential effects of activity reductions and dietary changes associated with the obesity epidemic and COVID-19 pandemic.

Care of infants is a hallmark of mammals. Whereas parental care by mothers is obligatory for offspring survival in virtually all mammals, fathers provide care for their offspring in only an estimated 5%-10% of genera. In these species, the transition into fatherhood is often accompanied by pronounced changes in males' behavioral responses to young, including a reduction in aggression toward infants and an increase in nurturant behavior. The onset of fatherhood can also be associated with sensory, affective, and cognitive changes. The neuroplasticity that mediates these changes is not well understood; however, fatherhood can alter the production and survival of new neurons; function and structure of existing neurons; morphology of brain structures; and neuroendocrine signaling systems. Although these changes are thought to promote infant care by fathers, very little evidence exists to support this hypothesis; in most cases, neither the mechanisms underlying neuroplasticity in fathers nor its functional significance is known. In this paper, we review the available data on the neuroplasticity that occurs during the transition into fatherhood. We highlight gaps in our knowledge and future directions that will provide key insights into how and why fatherhood alters the structure and functioning of the male brain.

In male mammals that provide care for their offspring, fatherhood can lead to changes in behavioral, morphological, and physiological traits, some of which might constitute trade-offs. However, relatively little is known about these changes, especially across multiple reproductive bouts, which are expected to magnify differences between fathers and nonreproductive males. We evaluated consequences of fatherhood in the monogamous, biparental California mouse (

California mice (Peromyscus californicus) differ from most other mammals in that they are biparental, genetically monogamous, and (compared with other Peromyscus) relatively large. We evaluated effects of cold acclimation on metabolic rate, exercise performance, and morphology of pair-housed male California mice, as well as modulation of these effects by fatherhood. In Experiment 1, virgin males housed at 5° or 10°C for approximately 25days were compared with virgins housed at standard vivarium temperature of 22°C. Measures included resting metabolic rate (RMR), maximal oxygen consumption ([Formula: see text]max), grip strength, and sprint speed. In Experiment 2, virgin males housed at 22°C were compared with three groups of males housed at 10°C: virgins, breeding males (housed with a female and their pups), and non-breeding males (housed with an ovariectomized, estrogen- and progesterone-treated female) after long-term acclimation (mean 243days). Measures in this experiment included basal metabolic rate (BMR), [Formula: see text]max, maximal thermogenic capacity ([Formula: see text]sum), and morphological traits. In Experiment 1, virgin males housed at 5° and 10°C had higher RMR and [Formula: see text]max than those at 22°C. In Experiment 2, 10°C-acclimated groups had shorter bodies; increased body, fat, and lean masses; higher BMR and [Formula: see text]sum, and generally greater morphometric measures and organ masses than virgin males at 22°C. Among the groups housed at 10°C, breeding males had higher BMR and lower [Formula: see text]max than non-breeding and/or virgin males. Overall, we found that effects of fatherhood during cold acclimation were inconsistent, and that several aspects of cold acclimation differ substantially between California mice and other small mammals.

Although behavior may often be a fairly direct target of natural or sexual selection, it cannot evolve without changes in subordinate traits that cause or permit its expression. In principle, changes in endocrine function could be a common mechanism underlying behavioral evolution because they are well positioned to mediate integrated responses to behavioral selection. More specifically, hormones can influence both motivational (e.g., brain) and performance (e.g., muscles) components of behavior simultaneously and in a coordinated fashion. If the endocrine system is often “used” as a general mechanism to effect responses to selection, then correlated responses in other aspects of behavior, life history, and organismal performance (e.g., locomotor abilities) should commonly occur because any cell with appropriate receptors could be affected. Ways in which behavior coadapts with other aspects of the phenotype can be studied directly through artificial selection and experimental evolution. Several studies have targeted rodent behavior for selective breeding and reported changes in other aspects of behavior, life history, and lower-level effectors of these organismal traits, including endocrine function. One example involves selection for high levels of voluntary wheel running, one aspect of physical activity, in four replicate High Runner (HR) lines of mice. Circulating levels of several hormones (including insulin, testosterone, thyroxine, triiodothyronine) have been characterized, three of which—corticosterone, leptin, and adiponectin—differ between HR and control lines, depending on sex, age, and generation. Potential changes in circulating levels of other behaviorally and metabolically relevant hormones, as well as in other components of the endocrine system (e.g., receptors), have yet to be examined. Overall, results to date identify promising avenues for further studies on the endocrine basis of activity levels.

Although effects of motherhood on mothers have been well documented in mammals, the effects of fatherhood on fathers are not well known. We evaluated effects of being a father on key metabolic and performance measures in the California mouse, Peromyscus californicus. California mice are genetically monogamous in the wild, and fathers show similar parental behavior to mothers, with the exception of lactation. To investigate the impact of fatherhood on fathers, focal males were paired with an intact female (breeding males), a tubally ligated female (nonbreeding males), or another male (virgins). Starting 3-5 d after the birth of each breeding pair's first litter, males were tested for locomotor performance (maximum sprint speed, treadmill endurance), basal metabolic rate (BMR), and maximum oxygen consumption ([Formula: see text]). At the end of the 11-d test period, mice were euthanized, hematocrit was determined, and organs were weighed. Speed, endurance, and [Formula: see text] were significantly repeatable between two replicate measurement days but did not differ among groups, nor did BMR. Breeding males had significantly larger hind limb muscles than did nonbreeding males, whereas virgin males had heavier subcutaneous fat pads than did nonbreeding and breeding males. Several correlations were observed at the level of individual variation (residuals from ANCOVA models), including positive correlations for endurance with [Formula: see text], [Formula: see text] with testes mass, and some of the digestion-related organs with each other. These results indicate that fatherhood may not have pronounced performance, metabolic, or morphological effects on fathers, at least under standard laboratory conditions and across a single breeding cycle.

Female mammals often demonstrate a rapid initiation of maternal responsiveness immediately after giving birth, as a result of neuroendocrine changes that occur during pregnancy and parturition. However, fathers and virgins of some species may display infant care similar to that performed by mothers but without experiencing these physiological events. In biparental species, in which both mothers and fathers care for their offspring, both sex and age may affect parental motivation, even in adult virgins. We examined the effects of sex and age on parental motivation in the California mouse, a monogamous, biparental rodent. We compared parental motivation of male and female virgins in both mid- and old adulthood using two new tests - a T-maze test and a rain test - as well as in standard parental-behavior tests. Adult virgin males were more parentally motivated than adult virgin females in both the T-maze test and the parental-behavior test, but parental motivation did not differ markedly between middle-aged and older adults of either sex. These findings suggest that sex differences in parental motivation in adult virgins are similar to those observed in other biparental rodents, and indicate that the T-maze test may be useful for evaluating parental motivation in this species.

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.

Parental care by fathers enhances offspring survival and development in numerous species. In the biparental California mouse, Peromyscus californicus, behavioral plasticity is seen during the transition into fatherhood: adult virgin males often exhibit aggressive or indifferent responses to pups, whereas fathers engage in extensive paternal care. In this species and other biparental mammals, the onset of paternal behavior is associated with increased neural responsiveness to pups in specific brain regions, including the medial preoptic area of the hypothalamus (MPOA), a region strongly implicated in both maternal and paternal behavior. To assess possible changes in neural circuit properties underlying this increased excitability, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in adult male California mice that were either virgins or first-time fathers. We used standard whole-cell recordings in a novel in vitro slice preparation. Excitatory and inhibitory post-synaptic currents from MPOA neurons were recorded in response to local electrical stimulation, and input/output curves were constructed for each. Responses to trains of stimuli were also examined. We quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. Biocytin was injected into neurons during recording, and their morphology was analyzed. Most parameters did not differ significantly between virgins and fathers. However, we document a decrease in synaptic inhibition in fathers. These findings suggest that the onset of paternal behavior in California mouse fathers may be associated with limited electrophysiological plasticity within the MPOA.

Estrogen depletion leads to bone loss in almost all mammals with frequent regular ovarian cycles. However, subordinate adult female common marmosets (Callithrix jacchus) undergo socially induced anovulation and hypoestrogenism without clinically apparent adverse skeletal consequences. Thus, we speculated that this non human primate might have evolved a mechanism to avoid estrogen-depletion bone loss. To test this possibility, we performed three experiments in which lumbar-spine (L5-L6) bone mineral content (BMC) and density (BMD) were assessed using dual-energy X-ray absorptiometry: (i) cross-sectionally in 13 long-term ovariectomized animals and 12 age- and weight-matched controls undergoing ovulatory cycles; (ii) longitudinally in 12 animals prior to, 3-4 and 6-7 months following ovariectomy (ovx), and six controls; and (iii) cross-sectionally in nine anovulatory subordinate and nine dominant females. In Experiments 1 and 3, plasma estradiol and estrone concentrations were measured and uterine dimensions were obtained by ultrasound in a subset of animals as a marker of functional estrogen depletion. Estrogen levels, uterine trans-fundus width, and uterine dorso-ventral diameter were lower in ovariectomized and subordinate females than in those undergoing ovulatory cycles. However, no differences were found in L5-L6 BMC or BMD. These results indicate that estrogen depletion, whether surgically or socially induced, is not associated with lower bone mass in female common marmosets. Thus, this species may possess unique adaptations to avoid bone loss associated with estrogen depletion.

Ingestion of placenta by mammalian mothers can lead to changes in pain sensitivity, hormone levels, and behavioral responses to newborns. In some biparental mammals, males, in addition to females, ingest placenta when their offspring are born. In the monogamous, biparental California mouse (Peromyscus californicus), males first become attracted to placenta when cohabitating with their pregnant mate, and virgin males administered placenta are less neophobic than males given oil vehicle. In this study, we investigated the effects of placentophagia on pain sensitivity, anxiety-like behavior, behavioral responses to pups, and circulating corticosterone levels of both breeding and nonbreeding male California mice. We orally administered either a conspecific placenta or oil vehicle to male mice from three reproductive conditions (first-time fathers, first-time expectant fathers, and virgin males) and tested their pain sensitivity 1 h later, as well as their exploratory behavior and paternal responsiveness in an open field 4 h post-treatment. We measured plasma corticosterone immediately after the open-field test. We found that placenta-treated males, independent of reproductive condition, traveled significantly longer distances in the open field than males treated with oil, indicative of lower anxiety. Additionally, fathers had shorter latencies to approach and to care for pups (i.e., huddling and licking pups), and spent more time engaging in these behaviors, than did age-matched expectant fathers and virgin males, independent of treatment. We found no effect on plasma corticosterone levels or pain sensitivity as a result of either treatment or reproductive condition. These findings indicate that placenta ingestion decreases anxiety-related behaviors in male California mice, but might not influence pain sensitivity, paternal responsiveness, or plasma corticosterone concentrations.

Across the animal kingdom, parents in many species devote extraordinary effort toward caring for offspring, often risking their lives and exhausting limited resources. Understanding how the brain orchestrates parental care, biasing effort over the many competing demands, is an important topic in social neuroscience. In mammals, maternal care is necessary for offspring survival and is largely mediated by changes in hormones and neuropeptides that fluctuate massively during pregnancy, parturition, and lactation (e.g., progesterone, estradiol, oxytocin, and prolactin). In the relatively small number of mammalian species in which parental care by fathers enhances offspring survival and development, males also undergo endocrine changes concurrent with birth of their offspring, but on a smaller scale than females. Thus, fathers additionally rely on sensory signals from their mates, environment, and/or offspring to orchestrate paternal behavior. Males can engage in a variety of infant-directed behaviors that range from infanticide to avoidance to care; in many species, males can display all three behaviors in their lifetime. The neural plasticity that underlies such stark changes in behavior is not well understood. In this chapter we summarize current data on the neural circuitry that has been proposed to underlie paternal care in mammals, as well as sensory, neuroendocrine, and experiential influences on paternal behavior and on the underlying circuitry. We highlight some of the gaps in our current knowledge of this system and propose future directions that will enable the development of a more comprehensive understanding of the proximate control of parenting by fathers.

Reproduction strongly influences metabolism, morphology and behavior in female mammals. In species in which males provide parental care, reproduction might have similar effects on fathers. We examined effects of an environmental challenge on metabolically important physiological, morphological, and behavioral measures, and determined whether these effects differed between reproductive and non-reproductive males, in the biparental California mouse (Peromyscus californicus). Males were paired with an ovary-intact female, an ovariectomized female treated with estrogen and progesterone to induce estrus, or an untreated ovariectomized female. Within each group, half of the animals were housed under standard laboratory conditions and half in cages requiring them to climb wire towers to obtain food and water; these latter animals were also fasted for 24 hours every third day. We predicted that few differences would be observed between fathers and non-reproductive males under standard conditions, but that fathers would be in poorer condition than non-reproductive males under challenging conditions. Body and fat mass showed a housing condition x reproductive group interaction: the challenge condition increased body and fat mass in both groups of non-reproductive males, but breeding males were unaffected. Males housed under the physical and energetic challenge had higher blood lipid content, lower maximal aerobic capacity and related traits (hematocrit and relative triceps surae mass), increased pain sensitivity and increased number of fecal boli excreted during tail-suspension tests (a measure of anxiety), compared to controls. Thus, our physical and energetic challenge paradigm altered metabolism, morphology and behavior, but these effects were largely unaffected by reproductive condition.

© 2015 The Zoological Society of London. Studies of biparental mammals demonstrate that males may undergo systematic changes in body mass as a consequence of changes in reproductive status; however, these studies typically have not teased apart the effects of specific social and reproductive factors, such as cohabitation with a female per se, cohabitation with a breeding female specifically, and engagement in paternal care. We aimed to determine whether California mouse Peromyscus californicus fathers undergo systematic changes in body mass and if so, which specific social/reproductive factor(s) might contribute to these changes. We compared mean weekly body masses over a 5-week period in (1) males housed with another male versus males housed with a non-reproductive (tubally ligated) female; (2) males housed with a tubally ligated female versus males housed with a female that was undergoing her first pregnancy; (3) experienced fathers housed with versus without pups during their mate's subsequent pregnancy. Body mass did not differ between males housed with another male and those housed with a non-reproductive female; however, males housed with a non-reproductive female were significantly heavier than those housed with a primigravid female. Among experienced fathers, those housed with pups from their previous litter underwent significant increases in body mass across their mates' pregnancy, whereas fathers housed without pups did not. These results suggest that male body mass is reduced by cohabitation with a breeding (pregnant) female, but not by cohabitation with a non-reproductive female, and that increases in body mass across the mate's pregnancy are associated with concurrent care of offspring rather than cohabitation with a pregnant female. Additional work is needed to determine the mechanisms and functional significance, if any, of these changes in male body mass with reproductive condition.

Parental care by fathers, although rare among mmmals, can be essential for the survival and normal development of offspring in biparental species. A growing body of research on biparental rodents has identified several developmental and experiential influences on paternal responsiveness. Some of these factors, such as pubertal maturation, interactions with pups, and cues from a pregnant mate, contribute to pronounced changes in paternal responsiveness across the course of the lifetime in individual males. Others, particularly intrauterine position during gestation and parental care received during postnatal development, can have long-term effects on paternal behavior and contribute to stable differences among individuals within a species. Focusing on five well-studied, biparental rodent species, we review the developmental and experiential factors that have been shown to influence paternal responsiveness, and consider their roles in generating both intra- and inter-individual variation. We also review hormones and neuropeptides that have been shown to modulate paternal care and discuss their potential contributions to behavioral differences within and between males. Finally, we discuss the possibility that vasopressinergic and possibly oxytocinergic signaling within the brain, modulated by gonadal steroid hormones, may represent the “final common pathway” mediating effects of developmental and experiential variables on intra- and inter-individual variation in paternal care.

Physiological and affective condition can be modulated by the social environment and parental state in mammals. However, in species in which males assist with rearing offspring, the metabolic and affective effects of pair bonding and fatherhood on males have rarely been explored. In this study we tested the hypothesis that fathers, like mothers, experience energetic costs as well as behavioral and affective changes (e.g., depression; anxiety) associated with parenthood. We tested this hypothesis in the monogamous, biparental California mouse (Peromyscus californicus). Food intake, blood glucose and lipid levels, blood insulin and leptin levels, body composition, pain sensitivity, and depression-like behavior were compared in males from three reproductive groups: virgin males (VM, housed with another male), non-breeding males (NB, housed with a tubally ligated female), and breeding males (BM, housed with a female and their first litter). We found statistically significant (P < 0.007, when modified for Adaptive False Discovery Rate) or nominally significant (0.007 < P < 0.05) differences among reproductive groups in relative testis mass, circulating glucose, triglyceride, and insulin concentrations, pain sensitivity, and anxiety-like behaviors. A priori contrasts indicated that VM produced significantly more fecal pellets than BM in the tail-suspension test, had significantly higher glucose levels than NB, and had significantly lower average testis masses than did NB and BM. A priori contrasts also indicated that VM had a nominally longer latency to the pain response than NB and that VM had nominally higher insulin levels than did NB. For breeding males, litter size (one to three pups) was a nominally significant positive predictor of body mass, food consumption, fat mass, and plasma leptin concentration. These results indicate that cohabitation with a female and/or fatherhood influences several metabolic, morphological, and affective measures in California mouse males. Overall, the changes we observed in breeding males were minor, but stronger effects might occur in long-term breeding males and/or under more challenging environmental conditions.

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 minutes 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, and 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.

Motherhood is energetically costly for mammals and is associated with pronounced changes in mothers' physiology, morphology and behavior. In ~5% of mammals, fathers assist their mates with rearing offspring and can enhance offspring survival and development. Although these beneficial consequences of paternal care can be mediated by direct effects on offspring, they might also be mediated indirectly, through beneficial effects on mothers. We tested the hypothesis that fathers in the monogamous, biparental California mouse (Peromyscus californicus) reduce the burden of parental care on their mates, and therefore, that females rearing offspring with and without assistance from their mates will show differences in endocrinology, morphology and behavior, as well as in the survival and development of their pups. We found that pups' survival and development in the lab did not differ between those raised by a single mother and those reared by both mother and father. Single mothers spent more time in feeding behaviors than paired mothers. Both single and paired mothers had higher lean mass and/or lower fat mass and showed more anxiety-like behavior in open-field tests and tail-suspension tests, compared to non-breeding females. Single mothers had higher body-mass-corrected liver and heart masses, but lower ovarian and uterine masses, than paired mothers and/or non-breeding females. Mass of the gastrointestinal tract did not differ between single and paired mothers, but single mothers had heavier gastrointestinal tract compared to non-breeding females. Single motherhood also induced a flattened diel corticosterone rhythm and a blunted corticosterone response to stress, compared to non-breeding conditions. These findings suggest that the absence of a mate induces morphological and endocrine changes in mothers, which might result from increased energetic demands of pup care and could potentially help maintain normal survival and development of pups.

Parturient females ingest placenta in most mammalian species, whereas fathers may do so in species in which both parents provide care for their offspring. To determine if the propensity to eat placenta varies with reproductive status in the biparental California mouse, we presented placenta to virgin (housed with a same-sex pairmate), expectant (pregnant with their first litter), and multiparous adult males and females. Liver was presented identically, 3-7 days later, as a control. Multiparous females were more likely to eat placenta than expectant and virgin females (p-values

article i nfo Previous studies indicate that reproductive condition can alter stress response and glucocorticoid release. Al- though the functional significance of hypothalamic-pituitary-adrenal (HPA) axis modulation by breeding condition is not fully understood, one possible explanation is the behavior hypothesis, which states that an animal's need to express parental behavior may be driving modulation of the HPA axis. This possibility is con- sistent with findings of blunted activity and reactivity of the HPA axis in lactating female mammals; however, effects of reproductive status on HPA function have not been well characterized in male mammals that ex- press parental behavior. Therefore, we tested this hypothesis in the monogamous and biparental California mouse. Several aspects of HPA activity were compared in males from three reproductive conditions: virgin males (housed with another male), non-breeding males (housed with a tubally ligated female), and first-time fathers (housed with a female and their first litter of pups). In light of the behavior hypothesis we predicted that new fathers would differ from virgin and non-breeding males in several aspects of HPA function and corticosterone (CORT) output: decreased amplitude of the diurnal rhythm in CORT, a blunted CORT increase following predator-odor stress, increased sensitivity to glucocorticoid negative feedback, and/or a blunted CORT response to pharmacological stimulation. In addition, we predicted that first-time fa- thers would be more resistant to CORT-induced suppression of testosterone secretion, as testosterone is im- portant for paternal behavior in this species. We found that virgin males, non-breeding males and first-time fathers did not display any CORT differences in diurnal rhythm, response to a predator-odor stressor, or re- sponse to pharmacological suppression or stimulation. Additionally, there were no differences in circulating testosterone concentrations. Adrenal mass was, however, significantly lower in new fathers than in virgin or non-breeding males. These results suggest that the behavior hypothesis does not explain HPA function across reproductive conditions in male California mice.

The California mouse, Peromyscus californicus, is an increasingly popular animal model in behavioral, neural, and endocrine studies, but little is known about its baseline hypothalamicpituitary-adrenal (HPA) axis activity or HPA responses to stressors. We characterized plasma corticosterone (CORT) concentrations in P. californicus under baseline conditions across the diurnal cycle, in response to pharmacological manipulation of the HPA axis, and in response to a variety of stressors at different times of day. In addition, we explored the use of fecal samples to monitor adrenocortical activity non-invasively. California mice have very high baseline levels of circulating CORT that change markedly over 24 hours, but that do not differ between the sexes. This species may be somewhat glucocorticoid-resistant in comparison to other rodents as a relatively high dose of dexamethasone (5 mg/kg, s.c.) was required to suppress plasma CORT for 8 h post-injection. CORT responses to stressors and ACTH injection differed with time of day, as CORT concentrations were elevated more readily during the morning (inactive period) than in the evening (active period) when compared to time-matched control. Data from 3H-CORT injection studies show that the time course for excretion of fecal CORT, or glucocorticoid metabolites, differs with time of injection. Mice injected in the evening excreted the majority of fecal radioactivity 2–4 h post-injection whereas mice injected during the morning did so at 14–16 h post-injection. Unfortunately, the antibody we used does not adequately bind the most prevalent fecal glucocorticoid metabolites and therefore we could not validate its use for fecal assays.

The glucocorticoid hormones corticosterone (CORT) and cortisol influence numerous physiological, morphological, and behavioral functions. However, few studies have addressed possible relationships between individual differences in glucocorticoid concentrations and whole-animal performance or metabolism. Because CORT is important in glucose regulation and energy metabolism and can influence activity levels, we hypothesized that individual variation in baseline circulating CORT levels would correlate with individual differences in energy expenditure (routine and maximal), aerobic physiology, voluntary exercise on wheels, and organ masses. We tested this hypothesis in the California mouse (Peromyscus californicus). We collected data from 54 adult, colony-bred mice on baseline CORT levels (measured near both the circadian peak and the circadian trough), voluntary wheel running and its energetic costs, maximal oxygen consumption during forced treadmill exercise ([Formula: see text]), basal metabolic rate, and relative organ masses. We found surprisingly few statistically significant relationships among CORT, energy metabolism, behavior, and organ masses, and these relationships appeared to differ between males and females. These findings suggest that individual differences in baseline CORT levels are not an important determinant of voluntary activity levels or aerobic performance in California mice.

California mice Peromyscus californicus are a rodent species in which fathers provide extensive paternal care; however, behavioral responses of virgin males toward conspecific neonates vary from paternal behavior to tolerance to infanticide. Indirect evidence suggests that paternal responses might be influenced by social status potentially through increased stress and anxiety in subordinate males. To test this hypothesis, we housed 12 virgin male California mice in same-sex dyads on weaning and assessed their within-dyad subordinate or dominant status using food-competition and urine-marking tests. In addition, behavioral responses to an unrelated pup, expression of vasopressin (AVP) and corticotropin-releasing hormone (CRH) mRNA in the paraventricular hypothalamic nucleus (PVN), basal plasma levels of testosterone and corticosterone, and body mass were measured. Food-competition and urine-marking tests did not reveal strong or stable dominance-subordination relationships in male-male dyads. Latency to sniff a newborn pup was correlated negatively with urine marking in the center of a novel environment and positively with expression of AVP mRNA in the PVN. Because these three parameters are all associated with state anxiety in other rodent species, these results suggest that individual differences in paternal responsiveness may be influenced by individual differences in anxiety but not necessarily by social status in virgin male California mice.

Stress can inhibit maternal behaviour and increase rates of child abuse in humans and other animals; however, the neuroendocrine mechanisms are not known. To determine whether corticotrophin-releasing hormone (CRH) plays a role in stress-induced disruption of maternal behaviour in primates, we characterised the effects of acute i.c.v. infusions of CRH on maternal and abusive behaviour in common marmoset monkeys (Callithrix jacchus). Nulliparous females were implanted with indwelling i.c.v. guide cannulae before conception. Between 18 and 58 days after the birth of her first infants, each female underwent a series of i.c.v. infusions of human CRH (0, 2, 8 and 25 μg) in 8 μl of artificial cerebrospinal fluid. In the 70 min after infusion, marmosets were tested with one of their infants, first in their home cage and, subsequently, in an unfamiliar cage in which the infant was confined in a transparent box on the cage floor. In the home cage, the highest dose of CRH significantly reduced the amount of time that mothers spent carrying their infants, as compared to vehicle alone, although it did not reliably affect aggression toward the infant or other behaviours. In the confined-infant test, the highest dose of CRH significantly reduced the amount of time that mothers spent on the cage floor, increased mothers' vocalisation rates, and tended to reduce their activity levels and time spent in proximity to their infant. Twenty-five micrograms of CRH also elicited significant elevations in plasma adrenocorticotrophic hormone and cortisol concentrations compared to vehicle. These results indicate that i.c.v.-administered CRH reduces maternal behaviour in marmoset mothers, in both familiar and unfamiliar environments, but does not increase infant abuse.

In several mammalian species, hypothalamic-pituitary-adrenal (HPA) and behavioral responses to stressors are down-regulated in lactating females, possibly preventing stress-induced disruptions of maternal care. Experimental elevations of HPA axis hormones have been found to inhibit maternal behavior in lactating common marmoset monkeys ( Callithrix jacchus ), raising the question of whether lactating female marmosets also have blunted endogenous responses to stress. Therefore, we compared HPA and behavioral responses to standardized stressors in reproductively experienced female common marmosets that were undergoing ovulatory cycles and that either were (N = 7) or were not lactating (N = 8). Each marmoset underwent (1) a restraint stressor during the early follicular phase of the ovarian cycle (approximately 5 weeks postpartum for lactating females) and (2) exposure to a simulated hawk predator during the early to mid-luteal phase (approximately 7 weeks postpartum for lactating females). Lactating females were tested in the presence of one of their infants. Blood samples were collected before, during, and immediately after each test for determination of plasma adrenocorticotropic hormone (ACTH) and cortisol concentrations. Both stressors caused significant elevations in plasma ACTH and cortisol levels, and significant decreases in cortisol:ACTH ratios; however, lactating and non-lactating females showed no significant differences in their endocrine or behavioral responses to either stressor, or in baseline ACTH or cortisol levels. These findings suggest that in contrast to several other mammalian species, lactating female marmosets maintain full behavioral and HPA responsiveness to stress, at least in the presence of their infants.

Fathers play a substantial role in infant care in a small but significant number of mammalian species, including humans. However, the neural circuitry controlling paternal behavior is much less understood than its female counterpart. In order to characterize brain areas activated by paternal care, male California mice were separated from their female mate and litter for 3 h and then exposed to a pup or a control object (a glass pebble with the approximate size and oblong shape of a newborn pup) for 10 min. All males receiving a pup showed a strong paternal response towards it, whereas males receiving a pebble interacted with it only occasionally. Despite the clear behavioral differences, exposure to a pup did not increase Fos-like immunoreactivity (Fos-LIR) compared to a pebble in brain areas previously found to be associated with parental care, including the medial preoptic nucleus and medial bed nucleus of the stria terminalis. Pup exposure did, however, significantly increase Fos-LIR in the lateral habenula (LHb) and in predominantly serotonergic neurons in the caudal dorsal raphe nucleus (DRC), as compared to pebble exposure. Both the LHb and DRC are known to be involved in the behavioral responses to strong emotional stimuli; therefore, these areas might play a role in controlling parental behavior in male California mice.

Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and free-living subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females, however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus, reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.

© 2015 Elsevier Inc. This article is part of a Special Issue "Parental Care". Paternal care, though rare among mammals, is routinely displayed by several species of rodents. Here we review the neuroanatomical and hormonal bases of paternal behavior, as well as the behavioral and neuroendocrine consequences of paternal behavior for offspring. Fathering behavior is subserved by many of the same neural substrates which are also involved in maternal behavior (for example, the medial preoptic area of the hypothalamus). While gonadal hormones such as testosterone, estrogen, and progesterone, as well as hypothalamic neuropeptides such as oxytocin and vasopressin, and the pituitary hormone prolactin, are implicated in the activation of paternal behavior, there are significant gaps in our knowledge of their actions, as well as pronounced differences between species. Removal of the father in biparental species has long-lasting effects on behavior, as well as on these same neuroendocrine systems, in offspring. Finally, individual differences in paternal behavior can have similarly long-lasting, if more subtle, effects on offspring behavior. Future studies should examine similar outcome measures in multiple species, including both biparental species and closely related uniparental species. Careful phylogenetic analyses of the neuroendocrine systems presumably important to male parenting, as well as their patterns of gene expression, will also be important in establishing the next generation of hypotheses regarding the regulation of male parenting behavior.

SUMMARYRelationships among individual variation in exercise capacity, resting metabolism and morphology may offer insights into the mechanistic basis of whole-animal performance, including possible performance trade-offs (e.g. burst versus sustainable exercise, resting `maintenance' costs versus maximal power output). Although there have been several studies of correlations between performance, metabolism and morphology in fish, birds and squamate reptiles, relatively little work has been done with mammals. We measured several aspects of forced and voluntary locomotor performance in Mongolian gerbils (Meriones unguiculatus), along with minimal and maximal aerobic metabolic rates and organ sizes (mainly visceral organs and the musculoskeletal system). Maximal sprint and aerobic speeds and maximal oxygen consumption(V̇O2max) during forced exercise were similar to those of other small rodents; basal metabolic rate was below allometric predictions. At all tested speeds, voluntary running had a lower energy cost than forced treadmill running, due primarily to a higher zero-speed intercept of the speed-versus-power (oxygen consumption) relationship during forced running. Incremental costs of transport (slopes of speed-versus-power regressions) were slightly higher during voluntary exercise. Few of the correlations among performance variables, or between performance and organ morphology, were statistically significant. These results are consistent with many other studies that found weak correlations between organismal performance (e.g. V̇O2max) and putatively relevant subordinate traits, thus supporting the idea that some components within a functional system may exhibit excess capacity at various points in the evolutionary history of a population, while others constitute limiting factors.

Neonatal marmosets express an adrenal fetal zone comparable to humans. While adult males fail to express a functional ZR, with barely detectable blood DHEA levels, females produce higher levels of DHEA than males in adulthood. We investigated the presence of a putative functional ZR in adult female marmosets. In contrast to males, immunohistochemical analysis showed the ZR marker cytochrome b5 was elevated in the innermost zone in cycling females (compared to testis-intact males), further elevated in the adrenals from anovulatory females, and substantially elevated and continuous in ovariectomized females. As a functional test in vivo, following overnight dexamethasone treatment, cycling and anovulatory females showed higher levels of DHEA relative to males, but DHEA failed to increase in response to ACTH. In direct contrast, while ovariectomized females exhibited lower initial DHEA levels, clear increases were detectable after ACTH administration (p < 0.05), suggesting an adrenal origin. The apparent differences in cytochrome b5 expression between groups were also further verified by Western blotting of adrenal microsomes, and compared to 17,20-lyase activity; the two parameters were positively correlated (p < 0.01) across multiple treatment groups. We conclude that the cycling female marmoset expresses a rudimentary ZR with at least a capacity for DHEA production that becomes significantly ACTH-responsive after anovulation. Expression of cytochrome b5 in this region may be directly or indirectly controlled by gonadal function, and is, at least in part, a critical determinant in the development of an adrenal ZR that is more defined and significantly ACTH-responsive. © 2006 Elsevier Ireland Ltd. All rights reserved.

The hypothalamic-pituitary-adrenal (HPA) axis is important in regulating energy metabolism and in mediating responses to stressors, including increasing energy availability during physical exercise. In addition, glucocorticoids act directly on the central nervous system and influence behavior, including locomotor activity. To explore potential changes in the HPA axis as animals evolve higher voluntary activity levels, we characterized plasma corticosterone (CORT) concentrations and adrenal mass in four replicate lines of house mice that had been selectively bred for high voluntary wheel running (HR lines) for 34 generations and in four nonselected control (C) lines. We determined CORT concentrations under baseline conditions and immediately after exposure to a novel stressor (40 min of physical restraint) in mice that were housed without access to wheels. Resting daytime CORT concentrations were approximately twice as high in HR as in C mice for both sexes. Physical restraint increased CORT to similar concentrations in HR and C mice; consequently, the proportional response to restraint was smaller in HR than in C animals. Adrenal mass did not significantly differ between HR and C mice. Females had significantly higher baseline and postrestraint CORT concentrations and significantly larger adrenal glands than males in both HR and C lines. Replicate lines showed significant variation in body mass, length, baseline CORT concentrations, and postrestraint CORT concentrations in one or both sexes. Among lines, both body mass and length were significantly negatively correlated with baseline CORT concentrations, suggesting that CORT suppresses growth. Our results suggest that selection for increased locomotor activity has caused correlated changes in the HPA axis, resulting in higher baseline CORT concentrations and, possibly, reduced stress responsiveness and a lower growth rate.

Behaviorally subordinate female marmosets undergo social suppression of ovulation and hypoestrogenism, as well as chronic reductions in circulating basal cortisol concentrations. Because estrogen elevates hypothalamic-pituitary-adrenal axis activity and circulating glucocorticoid levels in other species, we tested the hypothesis that socially induced hypoestrogenism contributes to cortisol reductions in subordinate female marmosets. We characterized morning basal plasma cortisol levels, as well as cortisol responses to exogenous adrenocorticotropic hormone (ACTH; 0, 1, or 10 microg/kg), in seven anovulatory subordinate females and six ovariectomized, non-subordinate females under two conditions: during long-term treatment with estradiol (E2) and control. Circulating E2 and cortisol levels were compared to those of six dominant females undergoing ovulatory cycles. Basal cortisol concentrations in the control condition were significantly lower in subordinates than in both dominant and ovariectomized females. E2 treatment elevated circulating E2 levels of subordinate and ovariectomized females into the range seen in dominant females but did not increase either mean basal or ACTH-stimulated cortisol levels. To the contrary, E2 treatment caused a decline in basal cortisol levels over time, especially in ovariectomized animals. These results indicate that treatment with exogenous estrogen does not elevate circulating cortisol levels in previously hypoestrogenemic female marmosets and, correspondingly that socially induced hypoestrogenism does not diminish cortisol levels in subordinate females.

Common marmosets, Callithrix jacchus, are usually characterized as singular cooperative breeders, with only a single, dominant female reproducing in each group. Anecdotal reports, however, have described two females breeding concurrently when an unrelated male joins their group. We tested the hypothesis that incorporation of an unrelated adult male into a family systematically leads to the onset of reproductive activity in a daughter and investigated the underlying mechanisms. We collected hormonal and behavioural data from mothers and their eldest daughters before and after the father was removed from the family and either replaced by an unrelated male (N ¼ 11) or immediately returned to the family (N ¼ 7). Variation between daughters in the occurrence of ovulatory cyclicity was not associated with the presence of an unrelated male but was closely linked to daughters’ relationships with their mothers: only anovulatory daughters behaved submissively towards their mothers. Daughters never engaged in sexual behaviour with their fathers, but most did so with unrelated males. Similarly, daughters never conceived in intact natal families but did so in eight of 11 families containing an unrelated male. In six of these families, the mother and daughter bred concurrently. Thus, incorporation of an unrelated adult male into a marmoset family may frequently lead to the onset of plural breeding by activating sexual behaviour in a daughter; however, daughters ovulate only if they are not behaviourally subordinate to their mothers. Therefore, both inbreeding avoidance and rank-related reproductive suppression may constrain reproduction in marmoset daughters and contribute to maintenance of singular breeding.

Urbanization brings the introduction of roads and anthropogenic noise. Noise has negative health outcomes across vertebrates. White's treefrogs (Litoria caerulea) exposed to ecologically relevant levels of traffic noise for one week had elevated circulating corticosterone levels and decreased sperm count and sperm viability relative to controls., Urbanization is a major driver of ecological change and comes with a suite of habitat modifications, including alterations to the local temperature, precipitation, light and noise regimes. Although many recent studies have investigated the behavioural and ecological ramifications of urbanization, physiological work in this area has lagged. We tested the hypothesis that anthropogenic noise is a stressor for amphibians and that chronic exposure to such noise leads to reproductive suppression. In the laboratory, we exposed male White's treefrogs, Litoria caerulea, to conspecific chorus noise either alone or coupled with pre-recorded traffic noise nightly for 1 week. Frogs presented with anthropogenic noise had significantly higher circulating concentrations of corticosterone and significantly decreased sperm count and sperm viability than did control frogs. These results suggest that in addition to having behavioural and ecological effects, anthropogenic change might alter physiology and Darwinian fitness. Future work should integrate disparate fields such as behaviour, ecology and physiology to elucidate fully organisms’ responses to habitat change.

© 2015 British Society for Neuroendocrinology. Fatherhood in biparental mammals is accompanied by distinct neuroendocrine changes in males, involving some of the same hormones involved in maternal care. In the monogamous, biparental California mouse (Peromyscus californicus), paternal care has been linked to changes in the central and/or peripheral availability of oestrogen, progesterone, vasopressin and oxytocin, although it is not known whether these endocrine fluctuations are associated with changes in receptor availability in the brain. Thus, we compared mRNA expression of oestrogen receptor (ER)α, progesterone receptor (PR), vasopressin receptor (V1a) and oxytocin receptor (OTR) in brain regions implicated in paternal care [i.e. medial preoptic area (MPOA)], fear [i.e. medial amygdala (MeA)] and anxiety [i.e. bed nucleus of the stria terminalis (BNST)] between first-time fathers (n = 8) and age-matched virgin males (n = 7). Males from both reproductive conditions behaved paternally towards unrelated pups, whereas fathers showed significantly shorter latencies to behave paternally and less time investigating pups. Furthermore, fathers showed significantly lower PR, OTR and V1a receptor mRNA expression in the BNST compared to virgins. Fathers also showed a marginally significant (P = 0.07) reduction in progesterone receptor mRNA expression in the MPOA, although fatherhood was not associated with any other changes in receptor mRNA in the MPOA or MeA. The results of the present study indicate that behavioural and endocrine changes associated with the onset of fatherhood, and/or with cohabitation with a (breeding) female, are accompanied by changes in mRNA expression of hormone and neuropeptide receptors in the brain.

© 2014 British Society for Neuroendocrinology. In the 5-10% of mammals in which both parents routinely provide infant care, fathers as well as mothers undergo systematic endocrine changes as they transition into parenthood. Although fatherhood-associated changes in such hormones and neuropeptides as prolactin, testosterone, glucocorticoids, vasopressin and oxytocin have been characterised in only a small number of biparental rodents and primates, they appear to be more variable than corresponding changes in mothers, and experimental studies typically have not provided strong or consistent evidence that these endocrine shifts play causal roles in the activation of paternal care. Consequently, their functional significance remains unclear. We propose that endocrine changes in mammalian fathers may enable males to meet the species-specific demands of fatherhood by influencing diverse aspects of their behaviour and physiology, similar to many effects of hormones and neuropeptides in mothers. We review the evidence for such effects, focusing on recent studies investigating whether mammalian fathers in biparental species undergo systematic changes in (i) energetics and body composition; (ii) neural plasticity, cognition and sensory physiology; and (iii) stress responsiveness and emotionality, all of which may be mediated by endocrine changes. The few published studies, based on a small number of rodent and primate species, suggest that hormonal and neuropeptide alterations in mammalian fathers might mediate shifts in paternal energy balance, body composition and neural plasticity, although they do not appear to have major effects on stress responsiveness or emotionality. Further research is needed on a wider variety of biparental mammals, under more naturalistic conditions, to more fully determine the functional significance of hormone and neuropeptide profiles of mammalian fatherhood and to clarify how fatherhood may trade off with (or perhaps enhance) aspects of organismal function in biparental mammals.

Socially subordinate female common marmoset monkeys undergo pronounced, chronic reductions in basal plasma cortisol levels, which appear to result both from socially induced suppression of reproductive hormones and from direct effects of social subordination. In this study, we tested the hypothesis that this cortisol suppression is mediated by reduced adrenocortical responsiveness to adrenocorticotropic hormone (ACTH). Dominant, subordinate, and ovariectomized females were given dexamethasone (5 mg/kg, IM), followed the next morning by human ACTH 1–39 (10 μg/kg, IV) or sterile saline (0.5 ml/kg, IV); blood samples were collected at −20 through 150 min from ACTH or saline treatment and assayed for cortisol. ACTH, but not saline, caused a marked elevation of plasma cortisol levels. Prior to ACTH treatment, dominant females tended to have higher dexamethasone-suppressed cortisol levels than subordinate and ovariectomized females. After ACTH treatment, dominant females had significantly higher cortisol concentrations, as well as higher peak and net integrated cortisol responses to ACTH, than did subordinate and ovariectomized animals; the latter two groups showed comparable cortisol responses to ACTH. These results suggest that dampened adrenocortical responsiveness to ACTH contributes to chronic reductions in cortisol levels in subordinate female marmosets and may be mediated by suppression of reproductive hormones.

This study investigated whether annual changes in physiology occur in individually housed squirrel monkeys (Saimiri sciureus). Physiological measures were monitored for 20 months. Over the course of the study, all individually housed males and females exhibited clear annual changes in gonadal and adrenal hormone levels, and males exhibited species-typical changes in body weight. Females exhibited a typical pattern of hormonal changes, with elevations in gonadal steroids occurring during the same months as elevations in cortisol. Males, however, exhibited an atypical pattern, as elevations in hormone levels were not synchronized with each other; rather, elevations in testosterone occurred out of phase with changes in cortisol and body weight. The timing of annual events in individually housed subjects was compared to that in nearby social groups, in which the timing of the breeding season from year to year was determined by social group formations and was outside the naturally occurring breeding season. Elevations of ovarian and adrenocortical hormones in individually housed females were synchronized with indices of breeding in heterosexual social groups. Similarly, weight gain in males was associated with elevations in cortisol and, as with socially housed males, tended to precede seasonal breeding in the social groups. In contrast, annual testosterone elevations for individually housed males were not synchronized with breeding in nearby social groups. We conclude that direct physical interaction is not required for the annual expression of breeding readiness. Synchrony of seasonality among squirrel monkeys may be accomplished by distant social cues in females, but males may require physical interaction for complete synchrony of annual physiological changes.

Socially subordinate female common marmosets (Callithrix jacchus) have markedly lower plasma cortisol levels than dominant females. Subordinate females also undergo hypoestrogenemic anovulation, and estrogen can elevate glucocorticoid levels. Therefore, we previously hypothesized that this cortisol difference is mediated by rank-related differences in reproductive hormones, probably estradiol. To test this possibility, we characterized the effects of the ovarian cycle and ovariectomy on plasma cortisol concentrations. Beginning in the early follicular phase, basal blood samples were collected from seven cycling female marmosets daily for 16 days and at 2- to 3-day intervals for another 16 days. Samples were collected identically from seven anovulatory subordinate females and seven long-term ovariectomized females. Cortisol levels changed reliably across the ovarian cycle, with levels in the mid- to late follicular, peri-ovulatory, and early luteal phases higher than those in the remainder of the cycle. Cortisol levels of cycling females were significantly higher than those of subordinates at all parts of the cycle, but were significantly higher than those of ovariectomized females only during the midcycle elevation. Unexpectedly, subordinates had significantly lower cortisol levels than ovariectomized females, as well as higher estradiol and estrone levels and lower progesterone and luteinizing hormone (LH) levels. These results confirm that circulating cortisol concentrations are modulated by reproductive function in female marmosets but also indicate that low cortisol levels in subordinate females cannot be attributed simply to hypoestrogenemia. Instead, other factors, such as direct effects of social subordination or suppression of LH levels, contribute to suppression of cortisol in subordinates.