Monogamous California Mouse Research Articles

A Comparison of Scent Marking between a Monogamous and Promiscuous Species of Peromyscus: Pair Bonded Males Do Not Advertise to Novel Females

Scent marking can provide behavioral and physiological information including territory ownership and mate advertisement. It is unknown how mating status and pair cohabitation influence marking by males from different social systems. We compared the highly territorial and monogamous California mouse (Peromyscus californicus) to the less territorial and promiscuous white-footed mouse (P. leucopus). Single and mated males of both species were assigned to one of the following arenas lined with filter paper: control (unscented arena), male scented (previously scent-marked by a male conspecific), or females present (containing females in small cages). As expected, the territorial P. californicus scent marked and overmarked an unfamiliar male conspecific's scent marks more frequently than P. leucopus. Species differences in responses to novel females were also found based on mating status. The presence of unfamiliar females failed to induce changes in scent marking in pair bonded P. californicus even though virgin males increased marking behavior. Pair bonding appears to reduce male advertisement for novel females. This is in contrast to P. leucopus males that continue to advertise regardless of mating status. Our data suggest that communication through scent-marking can diverge significantly between species based on mating system and that there are physiological mechanisms that can inhibit responsiveness of males to female cues.

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.

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.

Sex Differences in Social Interaction Behavior Following Social Defeat Stress in the Monogamous California Mouse (Peromyscus californicus)

Stressful life experiences are known to be a precipitating factor for many mental disorders. The social defeat model induces behavioral responses in rodents (e.g. reduced social interaction) that are similar to behavioral patterns associated with mood disorders. The model has contributed to the discovery of novel mechanisms regulating behavioral responses to stress, but its utility has been largely limited to males. This is disadvantageous because most mood disorders have a higher incidence in women versus men. Male and female California mice (Peromyscus californicus) aggressively defend territories, which allowed us to observe the effects of social defeat in both sexes. In two experiments, mice were exposed to three social defeat or control episodes. Mice were then behaviorally phenotyped, and indirect markers of brain activity and corticosterone responses to a novel social stimulus were assessed. Sex differences in behavioral responses to social stress were long lasting (4 wks). Social defeat reduced social interaction responses in females but not males. In females, social defeat induced an increase in the number of phosphorylated CREB positive cells in the nucleus accumbens shell after exposure to a novel social stimulus. This effect of defeat was not observed in males. The effects of defeat in females were limited to social contexts, as there were no differences in exploratory behavior in the open field or light-dark box test. These data suggest that California mice could be a useful model for studying sex differences in behavioral responses to stress, particularly in neurobiological mechanisms that are involved with the regulation of social behavior.

Sex differences in hormonal responses to social conflict in the monogamous California mouse

Monogamous species are usually considered to be less likely to exhibit sex differences in behavior or brain structure. Most previous studies examining sex differences in stress hormone responses have used relatively sexually dimorphic species such as rats. We examined the stress hormone responses of monogamous California mice ( Peromyscus californicus) to resident-intruder tests. We also tested males and females under different photoperiods, because photoperiod has been shown to affect both aggression and stress hormone responses. Females, but not males showed a significant increase in corticosterone levels immediately following a resident-intruder test. Males but not females showed elevated corticosterone levels under short days. Females tested in aggression tests also showed a significant increase in plasma oxytocin levels, but only when housed in long days. This was consistent with our observation that females but not males had more oxytocin positive cells in the paraventricular nucleus (PVN) when housed under long days. Our data show that sex differences in glucocorticoid responses identified in other rodents are present in a monogamous species.

Prolonged separation delays wound healing in monogamous California mice, Peromyscus californicus, but not in polygynous white-footed mice, P. leucopus

Social interactions are often stressful, but under certain circumstances, they may be beneficial for health and well-being. In a previous study, wound healing was slowed after mate separation (2 days) in monogamous California mice, Peromyscus californicus, but not polygynous white-footed mice, P. leucopus. Although these results indicate that positive social interaction is critical for immune activity in some species, the extent to which such social effects are enduring remains unspecified. The goal of the present experiments was to determine whether a period representing ∼20% of expected adult lifespan of these species in the wild (8 weeks) would affect wound healing. Because our experimental design required that the same animals were wounded twice, we were also able to determine the extent to which wound healing is repeatable. Wound healing remained delayed after 8 weeks of separation in P. californicus, and healing scores were not correlated between first and second wounds within individuals. In P. leucopus however, housing conditions did not influence wound healing, but first and second wound healings were correlated indicating repeatability. In sum, our results suggest that positive social interactions may be important for promoting immune activity in some species.

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse ( Peromyscus californicus)

In the laboratory rat and mouse, neonatal handling enhances hippocampal-dependent learning in adulthood, an effect mediated by changes in maternal behavior toward the handled young. In the present study, we examined the interaction between neonatal handling and biparental care during the early postnatal period and its effect on cognitive function in adult California mice ( Peromyscus californicus). We characterized the parental behavior of handled and nonhandled father-present and father-absent families over the first 15 days of life. We then assessed cognitive performance of male and female offspring in the Barnes maze and object recognition test after they were 60 days of age. We found that the amount of licking and grooming received by pups was decreased in father-absent families. By postnatal days 12–15, licking and grooming in handled, father-absent families were equivalent to that of nonhandled, father-present families. Handling enhanced novel object recognition in father-present male mice with no effect in females. In the nonhandled group, the presence of the father had no effect on object recognition learning in male or female mice. Handling also enhanced spatial learning in the Barnes maze. In nonhandled families, the presence of the father appeared to have no effect on spatial learning in the male offspring. Interestingly, spatial learning in nonhandled, father-absent, female offspring was similar to that of handled animals. The average amount of licking and grooming received by pups was negatively correlated with the average number of errors made on the first day of reversal training in the Barnes maze. These data support previous findings that neonatal handling facilitates learning and memory in adulthood, suggest that under certain environmental conditions, there is a sex difference in the response of pups to paternal care, and further demonstrate the importance of active parental investment for offspring cognitive development.

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

The importance of paternal care on pup survival and pup growth in Peromyscus californicus when required to work for food

We examined paternal care in the monogamous California mouse when wheel running was necessary to obtain food. Paternal and maternal care, pup survival and feeding were compared in litters with single females (Male Absent) and paired females (Male Present) under three different foraging requirements. When wheel running was required for obtaining food (Wheel Contingent), the male's presence significantly increased pup survival. There were no significant effects of the male's presence on pup survival in the No Wheel (standard laboratory housing with ad lib food) or Wheel Noncontingent (running wheel with ad lib food) groups. Males may have indirectly increased pup survival by helping generate food through wheel running and then subsequently spending less time eating than females. While females reduced the time spent in parental care as pups aged, males increased the time spent in parental care as pups aged. Thus as pups became larger and more expensive to rear, the male increased parental care. These results indicate that paternal care benefits pup survival more under conditions where the parents must forage to obtain food than when food is provided ad lib in the standard laboratory environment.

Vasopressin and Aggression in Cross-Fostered California Mice (Peromyscus californicus) and White-Footed Mice (Peromyscus leucopus)

To examine how developmental experiences alter neural pathways associated with adult social behavior, we cross-fostered pups between the more aggressive and monogamous California mouse (Peromyscus californicus) and the less aggressive and polygamous white-footed mouse (P. leucopus). Cross-fostered males became more like their foster parents when tested as adults. Male white-footed mice became more aggressive only in an aggression test in a neutral arena, whereas the territorial California mice became less aggressive in resident–intruder aggression test, as measured by attack latency. Only the species that displayed a change in resident–intruder aggression showed a change in arginine vasopressin (AVP) levels: cross-fostered California mice had significantly lower levels of AVP-immunoreactive (AVP-ir) staining than controls in the bed nucleus of the stria terminalis (BNST) and the supraoptic nucleus (SON) and a nonsignificant trend toward lower levels in the medial amygdala (MA). Neither species showed changes in AVP-ir staining in a control area, the paraventricular nucleus (PVN). The changes in AVP-ir staining in the BNST and SON may not be caused by stress because cross-fostering was not associated with changes in adult plasma concentrations of two steroid hormones, corticosterone and testosterone, that have been associated with stress-related alterations in AVP pathways. These results suggest that manipulating the early parental environment can directly alter both a neurotransmitter system and species-typical patterns of social behavior, but that these effects may vary between species and under different social contexts.

Effects of morphine on electrically evoked contractions of the vas deferens in two congeneric rodent species differing in sperm competition intensity.

An early prediction of sperm competition theory was that males should adjust the number of sperm they deliver according to the risk of double mating and this has received empirical support in recent years. It has been suggested that adaptive regulation of sperm delivery in mammals may depend on changes in vas deferens contractility. In laboratory mice, the vas deferens is sensitive to opioid agonists and the secretion of endogenous opioid peptides can be affected by social interactions that may be predictive of sperm competition risk. The present experiment was conducted to determine whether morphine, an opioid agonist (at the mu-receptor), has different effects on electrically evoked contractions of the isolated vas deferens in two congeneric rodent species differing in sperm competition intensity. Morphine inhibited contractions of the vas deferens in the non-monogamous deer mouse (Peromyscus maniculatus) but not the monogamous California mouse (Peromyscus californicus). This implies that the vas deferens of P. maniculatus possesses functional mu-receptors and, thus, should be able to respond to changes in the circulating levels of endogenous agonists whose secretion can be affected by social interactions predictive of sperm competition risk.

Female sand gobies prefer good fathers over dominant males

Female preference for males successful in male–male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra– and intersexual selection in the sand goby, Pomatoschistus minutus , a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the ‘best’ males.

Helpers liberate female fairy-wrens from constraints on extra-pair mate choice

In cooperatively breeding superb fairy-wrens (Malurus cyaneus), all males contribute to the feeding and defence of young. Despite the expectation that such paternal care should be directed only to relatives, DNA fingerprinting revealed that most offspring (76%, 138 out of 181) were sired by extra-group males that contributed no care, and that almost all broods (95%, 38 out of 40) contained young sired by extra-group fathers. This is the highest known incidence of cuckoldry. This remarkable mating system is produced by female control of fertilization and consistent preference for certain extra-group male genotypes. This choice leads to the production of sons that also gain extra-group fertilizations. One constraint on the extra-pair mate choice of females is the level of parental assistance received from males. Males living in pairs contribute relatively more parental care and are more likely to gain paternity in one of their broods (85%, 11 out of 13) than dominant males in multi-male cooperative groups (30%, 8 out of 27). In groups helpers compensate for the lower parental assistance of dominant males, so the total feeding rate is similar between pairs and groups. This suggests that females allow males in pairs more paternity to ensure their assistance with parental care. Helpers provide an alternative source of paternal investment, and allow females to express unrestricted mate choice. Mating options for females in other species with female control of fertilization may also reflect a trade-off between acquiring the genes of high-quality males for their offspring and parental care of those offspring.

The stability of female social and mating preferences in the monogamous California mouse, Peromyscus californicus

Abstract. The stability of female social preferences for a male and its effect on subsequent mate preference was examined in the monogamous Peromyscus californicus by giving virgin females a choice of two tethered or yoke-restrained virgin males. Females were tested twice for 24 h with the same two males, first when not in oestrus and again during oestrus. In three experiments, females demonstrated significant social (association) preferences for a male within 24 h after first introduction. The vast majority of females maintained their initial social preference for the same male from the non-oestrous to the oestrous test, regardless of whether they were separated from males (experiment 1) or had constant access to males (experiments 2 and 3) between tests. Almost one third of all females, however, either reversed their initial preference or spent equal amounts of time in proximity to both males during the oestrous test. More than half of all females did not mate. Of the females that mated, only about 60% copulated with their preferred social partner. Thus, a female's social preference was not a reliable indicator of her mating preference. These results suggest that the link between female social and mating preferences may be established in the wild, in part, by a lack of opportunity to associate and mate with more than one male and that females may be reluctant to reproduce until the pair bond is well established.

Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse, Peromyscus californicus

Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse, Peromyscus californicus

The significance of father's presence for offspring survival in the monogamous California mouse, Peromyscus californicus

Abstract. The effects of male removal on offspring survival and growth were examined in Peromyscus californicus under three laboratory conditions: (1) warm ambient temperatures with food and water freely available, (2) warm ambient temperatures when parents were required to forage for food (i.e. wheel running) and (3) cold ambient temperatures with food and water freely available. The presence of the father had no effect on offspring survival in warm ambient temperatures, but father's presence enhanced infant survivorship in cold ambient temperatures and when parents had to forage to obtain food. Infants that survived, with or without their father, were similar in body mass from birth to weaning. Male care has probably evolved in P. californicus because paternal investment enhances offspring survival under natural conditions.

Mechanisms of sexual fidelity in the monogamous California mouse, Peromyscus californicus

Peromyscus californicus are exclusively monogamous in the wild. We examined in the laboratory whether established pairs of male and female P. californicus would remain faithful when given the opportunity to mate with an opposite sex stranger, either in the presence or absence of their partner. When the partner was present she or he was tethered and could not intervene. Females in postpartum estrus (day 0 postpartum) preferred to associate with their pairmate rather than the unfamiliar virgin male. Females also preferred to mate with their partner, but 15–20% of the females mated with the unfamiliar male both in the presence and absence of their partner. Paired males were tested with an unfamiliar, sexually inexperienced estrous female on days 4 and 8 postpartum with their partners either absent or present but not in postpartum estrus, and on day 0 in the absence of their partner. Males preferred to associate with their pairmate. Contrary to theoretical expectations, males did not copulate with the estrous female when given the opportunity regardless of whether their partner was present or not. Furthermore, few males (2/13) tested in the absence of their partner mated with a sexually experienced, postpartum estrous female. These results indicate that monogamy in P. californicus is maintained by a strong attraction and preference of pairmates for each other and by self-restraint from mating with others. Male mate guarding may further ensure female faithfulness. Males exhibit apparently more sexual fidelity than females.

Parental influences on female puberty in the monogamous California mouse, Peromyscus californicus

Sexual maturation of juvenille Peromyscus californicus females was delayed if females were housed with both parents. This delay was attributed to contact with the mother rather than the father. Sexual maturation was not affected by contact with a strange male, but puberty was delayed by contact with a strange female. In subsequent studies, the role of maternal urinary chemosignals and physical contact in delaying puberty was examined. Exposure to maternal urine or soiled bedding had no effect on sexual maturation in juvenile females. Puberty was delayed in juvenile females that had direct physical contact with their mother compared with females not exposed to their mother. Females exposed to their mother, but prevented physical contact by a double wire-mesh barrier, showed an intermediate delay in sexual maturation which did not differ significantly from either the contact or unexposed females. Thus physical contact with the mother and not a urinary chemosignal per se is necessary to delay sexual maturation in P. californicus.