The parental umwelt: Effects of parenthood on sensory processing in rodents.

An animal's umwelt, comprising its perception of the sensory environment, which is inherently subjective, can change across the lifespan in accordance with major life events. In mammals, the onset of motherhood, in particular, is associated with a neural and sensory plasticity that alters a mother's detection and use of sensory information such as infant-related sensory stimuli. Although the literature surrounding mammalian mothers is well established, very few studies have addressed the effects of parenthood on sensory plasticity in mammalian fathers. In this review, we summarize the major findings on the effects of parenthood on behavioural and neural responses to sensory stimuli from pups in rodent mothers, with a focus on the olfactory, auditory, and somatosensory systems, as well as multisensory integration. We also review the available literature on sensory plasticity in rodent fathers. Finally, we discuss the importance of sensory plasticity for effective parental care, hormonal modulation of plasticity, and an exploration of temporal, ecological, and life-history considerations of sensory plasticity associated with parenthood. The changes in processing and/or perception of sensory stimuli associated with the onset of parental care may have both transient and long-lasting effects on parental behaviour and cognition in both mothers and fathers; as such, several promising areas of study, such as on the molecular/genetic, neurochemical, and experiential underpinnings of parenthood-related sensory plasticity, as well as determinants of interspecific variation, remain potential avenues for further exploration.

Neural responses to pup calls and pup odors in California mouse fathers and virgin males.

The onset of mammalian maternal care is associated with plasticity in neural processing of infant-related sensory stimuli; however, little is known about sensory plasticity associated with fatherhood. We quantified behavioral and neural responses of virgin males and new fathers to olfactory and auditory stimuli from young, unfamiliar pups in the biparental California mouse (Peromyscus californicus). Each male was exposed for 10 min to one of four combinations of a chemosensory stimulus (pup-scented or unscented cotton [control]) and an auditory stimulus (pup vocalizations or white noise [control]). Behavior did not differ between fathers and virgins during exposure to sensory stimuli or during the following hour; however, males in both groups were more active both during and after exposure to pup-related stimuli compared to control stimuli. Fathers had lower expression of Fos in the main olfactory bulbs (MOB) but higher expression in the medial preoptic area (MPOA) and bed nucleus of the stria terminalis medial division, ventral part (STMV) compared to virgins. Lastly, males had higher Fos expression in MPOA when exposed to pup odor compared to control stimuli, and when exposed to pup odor and pup calls compared to pup calls only or control stimuli. These findings suggest that the onset of fatherhood alters activity of MOB, MPOA and STMV and that pup odors and vocalizations have additive or synergistic effects on males' behavior and MPOA activation.

Specificity of California mouse pup vocalizations in response to olfactory stimuli.

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.

Acute inhibition of dopamine ß-hydroxylase attenuates behavioral responses to pups in adult virgin California mice (Peromyscus californicus).

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 ß-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.

Effects of early-life exposure to Western diet and voluntary exercise on adult activity levels, exercise physiology, and associated traits in selectively bred High Runner mice.

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.

Plasticity of the paternal brain: Effects of fatherhood on neural structure and function.

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.

Effects of sex and age on parental motivation in adult virgin California mice.

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.

Long-Term Effects of Fatherhood on Morphology, Energetics, and Exercise Performance in California Mice (Peromyscus californicus).

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 (Peromsycus californicus) across seven consecutive reproductive bouts. We compared breeding adult males (housed with sham-ovariectomized females) with two control groups: nonbreeding males (housed with ovariectomized females treated with estrogen and progesterone to induce estrous behavior) and virgin males (housed with untreated ovariectomized females). At five time points (before pairing, early postpartum of the first litter, late postpartum of the second litter, early postpartum of the sixth litter, and late postpartum of the seventh litter or comparable time points for nonbreeding and virgin males), we measured males' body composition, hematocrit, predatory aggression, resting metabolic rate, maximal oxygen consumption (V˙O2 max⁡), grip strength, and sprint speed. We also weighed organs at the final time point. We predicted that fathers would have lower relative body fat and lower performance abilities compared with control groups and that these effects would become more pronounced with increasing parity. Contrary to predictions, breeding and control males differed in surprisingly few measures, and the number and magnitude of differences did not increase with parity. Thus, our expectations regarding trade-offs were not met. As reported in studies of single reproductive events, these results suggest that fatherhood has few costs in this species when housed under standard laboratory conditions, even across multiple reproductive bouts.

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.

Effects of single parenthood on mothers' behavior, morphology, and endocrine function in the biparental California mouse.

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.

Effects of short- and long-term cold acclimation on morphology, physiology, and exercise performance of California mice (Peromyscus californicus): potential modulation by fatherhood.

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 25 days 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 243 days). 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.

Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of 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.

Maintenance of bone mass despite estrogen depletion in female common marmoset monkeys (Callithrix jacchus).

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.

Neural Regulation of Paternal Behavior in Mammals: Sensory, Neuroendocrine, and Experiential Influences on the Paternal Brain.

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.

Behavioral and endocrine consequences of placentophagia in male California mice (Peromyscus californicus).

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.

Effects of a physical and energetic challenge on male California mice (Peromyscus californicus): modulation by reproductive condition.

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 h 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×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 with controls. Thus, our physical and energetic challenge paradigm altered metabolism, morphology and behavior, but these effects were largely unaffected by reproductive condition.

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation.

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.

Metabolic and affective consequences of fatherhood in male California mice.

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

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

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

Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior.

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.