Social Experience During Development and Female Offspring Aggression in Peromyscus Mice

Cross‐fostering between the highly aggressive, biparental California mouse (Peromyscus californicus) and the less aggressive, less parental white‐footed mouse (P. leucopus) influences female offspring attack latency in California mice, but not in white‐footed mice. Adult female California mice raised by white‐footed mice expressed longer attack latencies in a neutral‐arena test but not in a resident‐intruder test. One social cue that may be used by offspring to develop environmentally appropriate levels of aggression is the type of parental care during development. In California mice, a composite score of maternal behavior was positively associated with neutral‐arena aggression as indicated by decreased attack latency. In both species, paternal nest‐building was positively associated with neutral‐arena aggression and higher maternal retrieval behavior predicted higher offspring resident‐intruder aggression as indicated by decreased attack latency. Together, these results indicate that parental behavior has the potential to shape the development of attack latency in female offspring.     

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 20 min 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.     

The Association Between Male Offspring Aggression and Paternal and Maternal Behavior of Peromyscus Mice

Parents influence offspring aggression through genetic and non‐genetic mechanisms, although the latter are less well understood. To examine potential non‐genetic effects of parents on offspring, we cross‐fostered the highly aggressive and biparental California mouse (Peromyscus californicus) and the less aggressive, less parental white‐footed mouse (Peromyscus leucopus). In‐fostered animals within each species were used as controls. We examined associations between the foster parents’ behavior and aggression of the fostered male offspring in resident–intruder (R–I) and neutral arena aggression tests. When both species and fostering groups were combined, R–I aggression of offspring was positively associated with paternal time spent retrieving pups. In contrast, aggression in a neutral arena was negatively associated with a composite score of maternal behavior. We discuss how our findings regarding paternal retrievals may explain previously reported effects of cross‐fostering on male aggression.     

Effects of reproductive status on behavioral and endocrine responses to acute stress in a biparental rodent, the California mouse (Peromyscus californicus)

In several mammalian species, lactating females show blunted neural, hormonal, and behavioral responses to stressors. It is not known whether new fathers also show stress hyporesponsiveness in species in which males provide infant care. To test this possibility, we determined the effects of male and female reproductive status on stress responsiveness in the biparental, monogamous California mouse (Peromyscus californicus). Breeding (N = 8 females, 8 males), nonbreeding (N = 10 females, 10 males) and virgin mice (N = 12 females, 9 males) were exposed to a 5-min predator-urine stressor at two time points, corresponding to the early postpartum (5-7 days postpartum) and mid/late postpartum (19-21 days postpartum) phases, and blood samples were collected immediately afterwards. Baseline blood samples were obtained 2 days prior to each stress test. Baseline plasma corticosterone (CORT) concentrations did not differ among male or female groups. CORT responses to the stressor did not differ among female reproductive groups, and all three groups showed distinct behavioral responses to predator urine. Virgin males tended to increase their CORT response from the first to the second stress test, while breeding and nonbreeding males did not. Moreover, virgin and nonbreeding males showed significant behavioral changes in response to predator urine, whereas breeding males did not. These results suggest that adrenocortical responses to a repeated stressor in male California mice may be modulated by cohabitation with a female, whereas behavioral responses to stress may be blunted by parental status.     

The Deer Mouse (<Emphasis Type="Italic">Peromyscus maniculatus</Emphasis>) as an Enzootic Reservoir of Plague in California

It has long been theorized that deer mice (Peromyscus maniculatus) are a primary reservoir of Yersinia pestis in California. However, recent research from other parts of the western USA has implicated deer mice as spillover hosts during epizootic plague transmission. This retrospective study analyzed deer mouse data collected for plague surveillance by public health agencies in California from 1971 to 2016 to help elucidate the role of deer mice in plague transmission. The fleas most commonly found on deer mice were poor vectors of Y. pestis and occurred in insufficient numbers to maintain transmission of the pathogen, while fleas whose natural hosts are deer mice were rarely observed and even more rarely found infected with Y. pestis on other rodent hosts. Seroprevalence of Y. pestis antibodies in deer mice was significantly lower than that of several chipmunk and squirrel species. These analyses suggest that it is unlikely that deer mice play an important role in maintaining plague transmission in California. While they may not be primary reservoirs, results supported the premise that deer mice are occasionally exposed to and infected by Y. pestis and instead may be spillover hosts.     

Testosterone response to courtship predicts future paternal behavior in the California mouse, Peromyscus californicus

In the monogamous and biparental California mouse (Peromyscus californicus), paternal care is critical for maximal offspring survival. Animals form pair bonds and do not engage in extrapair matings, and thus female evaluation of paternal quality during courtship is likely to be advantageous. We hypothesized that male endocrine or behavioral response to courtship interactions would be predictive of future paternal behavior. To test this hypothesis, we formed 20 pairs of California mice, and evaluated their behavior during the first hour of courtship interactions and again following the birth of young. We also collected blood from males at baseline, 1 hr after pairing, 3 weeks paired, and when young were 4 days old to measure testosterone (T). We found that male T-response to courtship interactions predicted future paternal behavior, specifically the amount of time he huddled over young when challenged by the temporary removal of his mate. Males that mounted T increases at courtship also approached pups more quickly during this challenge than males who had a significant decrease in T at courtship. Proximity of the male and female during courtship predicted paternal huddling during a 1-hr observation, and a multiple regression analysis revealed that courtship behavior was also predictive of birth latency. We speculate that male T-response to a female in P. californicus is an honest indicator of paternal quality, and if detectable by females could provide a basis for evaluation during mate choice.     

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

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

Site fidelity and behavioral plasticity regulate an ungulate’s response to extreme disturbance

With rapid global change, the frequency and severity of extreme disturbance events are increasing worldwide. The ability of animal populations to survive these stochastic events depends on how individual animals respond to their altered environments, yet our understanding of the immediate and short‐term behavioral responses of animals to acute disturbances remains poor. We focused on animal behavioral responses to the environmental disturbance created by megafire. Specifically, we explored the effects of the 2018 Mendocino Complex Fire in northern California, USA, on the behavior and body condition of black‐tailed deer (Odocoileus hemionus columbianus). We predicted that deer would be displaced by the disturbance or experience high mortality post‐fire if they stayed in the burn area. We used data from GPS collars on 18 individual deer to quantify patterns of home range use, movement, and habitat selection before and after the fire. We assessed changes in body condition using images from a camera trap grid. The fire burned through half of the study area, facilitating a comparison between deer in burned and unburned areas. Despite a dramatic reduction in vegetation in burned areas, deer showed high site fidelity to pre‐fire home ranges, returning within hours of the fire. However, mean home range size doubled after the fire and corresponded to increased daily activity in a severely resource‐depleted environment. Within their home ranges, deer also selected strongly for patches of surviving vegetation and woodland habitat, as these areas provided forage and cover in an otherwise desolate landscape. Deer body condition significantly decreased after the fire, likely as a result of a reduction in forage within their home ranges, but all collared deer survived for the duration of the study. Understanding the ways in which large mammals respond to disturbances such as wildfire is increasingly important as the extent and severity of such events increases across the world. While many animals are adapted to disturbance regimes, species that exhibit high site fidelity or otherwise fixed behavioral strategies may struggle to cope with increased climate instability and associated extreme disturbance events.     

Differentiation of craniomandibular morphology in two sympatric <Emphasis Type="Italic">Peromyscus</Emphasis> mice (Cricetidae: Rodentia)

In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse) and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechanical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite force that is more suitable to access hard-shelled acorns despite its smaller body size.     

Pneumocystosis in wild small mammals from California

Cyst forms of the opportunistic fungal parasite Pneumocystis carinii were found in the lungs of 34% of the desert shrew, Notiosorex crawfordi (n = 59), 13% of the ornate shrew, Sorex ornatus (n = 55), 6% of the dusky-footed wood rat, Neotoma fuscipes (n = 16), 2.5% of the California meadow vole, Microtus californicus (n = 40), and 50% of the California pocket mouse, Chaetodipus californicus (n = 2) caught from southern California between February 1998 and February 2000. Cysts were not found in any of the harvest mouse, Reithrodontomys megalotis (n = 21), California mouse, Peromyscus californicus (n = 20), brush mouse, Peromyscus boylii (n = 7) or deer mouse, Peromyscus maniculatus (n = 4) examined. All infections were mild; extrapulmonary infections were not observed. Other lung parasites detected were Hepatozoon sp./spp. from M. californicus and Notiosorex crawfordi, Chrysosporium sp. (Emmonsia) from M. californicus, and a nematode from S. ornatus.     

Hormonal changes in mammalian fathers

Known and hypothesized relationships between steroid (estradiol, testosterone, and cortisol) and peptide (oxytocin, vasopressin, and prolactin) hormones and the expression of mammalian paternal behavior are reviewed. Emphasis is placed on newly emerging animal models, including nonhuman primates and men, with elaborate paternal behavior repertoires. Currently available data are broadly consistent with a working hypothesis that the expression of parental behavior will involve homologous neuroendocrine circuits in male and females. Understanding the neuroendocrinology of paternal behavior is an emerging research opportunity in behavioral neuroscience.     

Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors.

Previous comparative studies have suggested that the distribution of arginine vasopressin (AVP) pathways within the brain is associated with species-typical patterns of social behavior. In the current study, male parental behavior and aggression were compared in two species of Peromyscus. As predicted based on other studies, male mice from a monogamous species, the California mouse Peromyscus californicus, spent more time providing parental care to offspring than males from a polygamous species, the white-footed mouse Peromyscus leucopus. Sexually naive male California mice also attacked opponents more rapidly than white-footed mice during resident-intruder and neutral aggression tests. Since AVP has been shown to modulate these behaviors, we compared the distribution of vasopressinergic neurons and receptors. We predicted that greater AVP-immunoreactive (AVP-ir) staining in the bed nucleus of the stria terminalis and AVP receptor density in the lateral septum would occur in the species with low levels of paternal care because this pattern was found in similar comparisons with sexually naive monogamous and polygamous voles. In contrast, in our study, monogamous male mice showed more AVP-ir staining in the bed nucleus of the stria terminalis than the polygamous species, as well as more AVP receptors in the lateral septum. Parental behavior therefore does not appear to predict differences in patterns of AVP-ir staining and receptor distribution across species or vice versa. We propose the hypothesis that aggression may be better correlated with species patterns of AVP-ir staining density and receptor distribution.     

A positive Link Between Male Testosterone and Spacing Behavior in Pair‐Bonded California Mice

The effects of testosterone (T) on male sexual behavior are well established, but its roles in several associated social behaviors such as pair‐bonding and paternal behavior are diverse. Recently, we reported that male T in response to pairing with a female predicts future paternal behavior in the monogamous and biparental California mouse (Peromyscus californicus). Here, we examined whether T in response to pairing is also associated with spacing behavior between mates under laboratory conditions and if these behavioral patterns are continued during pup care. Pairs of California mice were observed throughout their pair bond before and again after pups were born. We found that males with higher T post‐pairing remained closer to their mates in the weeks before pups were born, and pairs with higher proximity measures during the pair bond spent more time caring for pups together. Overall, these results suggest a similar mechanism for spacing behavior across distinct phases of the pair bond.     

Increased vasopressin expression in the BNST accompanies paternally induced territoriality in male and female California mouse offspring

While developmental consequences of parental investment on species-typical social behaviors has been extensively characterized in same-sex parent-offspring interactions, the impact of opposite-sex relationships is less clear. In the bi-parental California mouse (Peromyscus californicus), paternal retrieval behavior induces territorial aggression and the expression of arginine vasopressin (AVP) in adult male offspring. Although similar patterns of territorially emerge among females, the sexually dimorphic AVP system has not been considered since it is generally thought to regulate male-typical behavior. However, we recently demonstrated that male and female P. californicus offspring experience increases in plasma testosterone following paternal retrieval. Since AVP expression is androgen-dependent during development, we postulate that increases in AVP expression may accompany territoriality in female, as well as male offspring. To explore this aim, adult P. californicus offspring that received either high or low levels of paternal care (retrievals) during early development were tested for territoriality and immunohistochemical analysis of AVP within the bed nucleus of the stria terminalis (BNST), paraventricular nucleus (PVN), and supraoptic nucleus (SON). Consistent with previous studies, high care offspring were more aggressive than low care offspring. Moreover, high care offspring had significantly more AVP immunoreactive (AVP-ir) cells within the BNST than low care offspring. This pattern was observed within female as well as male offspring, suggesting an equally salient role for paternal care on female offspring physiology. Regardless of early social experience, sex differences in AVP persisted in the BNST, with males having greater expression than females.     

Annual cyclicity of gall stone prevalence in deer mice (Peromyscus maniculatus gambelii)

The prevalence of gall stones (100% cholesterol) in a deer mouse (Peromyscus maniculatus) population located in Siskiyou County, California (USA) was studied on a monthly basis from February 1985 through January 1988. During each year we documented a pronounced annual cyclicity with peak prevalence (31 to 53%) during the winter and low prevalence (2 to 3%) during late summer. Gall stone prevalence was not related to sex or age of the animal. The earliest onset of gall stone production and the maximum prevalence achieved were associated with the greatest abundance of deer mice; lower levels of population abundance were associated with later onset of gall stone production and lower peak prevalences. This association of gall stone prevalence with both season and population abundance levels suggests that the causative factor(s) is/are related to the quality and availability of the diet.     

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

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

Compatibility drives female preference and reproductive success in the monogamous California mouse (Peromyscus californicus) more strongly than male testosterone measures

Female assessment of male attractiveness and how preferred qualities impact reproductive success is central to the study of mate choice. Male attractiveness may depend on traits beneficial to the reproductive success (RS) of any female, termed ‘universal quality’, and/or on behavioral and biological interactions between potential mates that reflect ‘compatibility’. The steroid hormone testosterone (T) often underlies male attractiveness in rodents and is associated with enhanced paternal care in the monogamous and biparental California mouse (Peromyscus californicus). We hypothesized that (1) T-characteristics are universally attractive to female California mice and that (2) if reproductive success is higher for females mated with preferred males, then females mated with males preferred by other females will also have higher reproductive success. Alternatively, we speculated that pair compatibility, based on emergent pair qualities, is important for a species with coordinated offspring care. We assessed individual T-characteristics in three ways: (1) T-response to GnRH challenges (2) baseline T-level and (3) T-response to a female. Testosterone-response did not predict female preference, but females spent more time investigating males with higher baseline T (accounting for only 9.6% of the variation in investigation time). None of the T-measures was associated with RS. Females paired with males they preferred produced litters more quickly and had higher RS than females paired with their non-preferred males. Naïve females who did not undergo preference tests had equivalent RS regardless of whether their mate was preferred or non-preferred by another female. These data suggest that higher male T elicits investigation, but female preference in the California mouse is more strongly linked with compatibility because individual preference was a better predictor of RS than any T measure.     

Harvesting sperm and artificial insemination of mice

Rodents of the genus Peromyscus (deer mice) are the most prevalent native North American mammals. Peromyscus species are used in a wide range of research including toxicology, epidemiology, ecology, behavioral, and genetic studies. Here they provide a useful model for demonstrations of artificial insemination. Methods similar to those displayed here have previously been used in several deer mouse studies, yet no detailed protocol has been published. Here we demonstrate the basic method of artificial insemination. This method entails extracting the testes from the rodent, then isolating the sperm from the epididymis and vas deferens. The mature sperm, now in a milk mixture, are placed in the female's reproductive tract at the time of ovulation. Fertilization is counted as day 0 for timing of embryo development. Embryos can then be retrieved at the desired time-point and manipulated.Artificial insemination can be used in a variety of rodent species where exact embryo timing is crucial or hard to obtain. This technique is vital for species or strains (including most Peromyscus) which may not mate immediately and/or where mating is hard to assess. In addition, artificial insemination provides exact timing for embryo development either in mapping developmental progress and/or transgenic work. Reduced numbers of animals can be used since fertilization is guaranteed. This method has been vital to furthering the Peromyscus system, and will hopefully benefit others as well.     

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

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

Patterns of parental care in two cricetid rodents, Onychomys torridus and Peromyscus leucopus

Daily observations were made of the maternal and paternal behaviour of Onychomys torridus and Peromyscus leucopus in laboratory cages. In both species, the females spent more time in the nest area with the young and groomed the young more frequently than their male partners, but the males played a surprisingly active role in nest attendance. Paternal nest attendance was more frequent in O. torridus males than in P. leucopus males. Onychomys males were also more active in grooming the young than Peromyscus males. These species-specific patterns of parental care are discussed in relation to the behavioural and ecological characteristics of Onychomys and Peromyscus.