Search

Paternal behaviour presumably evolved because male care of young was critical for offspring survival. We report field evidence indicating that paternal behaviour enhances offspring survival in a monogamous mammal, the biparental California mouse, Peromyscus californicus. Male removal resulted in lower offspring survival in father-absent than in father-present families. New males took up residence with widowed females, but usually after females had stopped lactating, suggesting that the importance of the father is not primarily protection against infanticidal intruders but rather direct care of young.

California mice (Peromyscus californicus) breed primarily during the winter rainy season and generally terminate breeding during the dry summer months. This pattern of reproduction could be regulated by day length, availability of green vegetation, or water availability. The effects of photoperiod and green vegetation on reproduction were examined in Experiment 1 by housing adult male P. californicus either in long (LD 14:10) or short (LD 8:16) photoperiods for 10 weeks with ad lib food and water availability. A subset of animals in each photoperiod treatment group also received supplements of fresh spinach thrice weekly. The effects of water availability were examined in Experiment 2 by housing adult males in long day length conditions for 10 weeks with ad lib or restricted (50% of ad lib) water availability. Neither photoperiod nor availability of green plant food significantly affected reproductive function in male California mice, although animals in long days with green food supplements displayed elevation of some reproductive organ masses. Short days did not suppress plasma LH or prolactin levels. Male P. californicus provide extensive care of the young during the short days of winter. The absence of photoperiod-induced changes in prolactin levels is consistent with the observation that elevated plasma prolactin titers are associated with male parental care in this species. In contrast, water restriction (simulated summer drought) reduced reproductive organ masses, as well as plasma levels of prolactin, and may act as an environmental cue to terminate breeding. Thus, water availability may regulate breeding in this species independently of photoperiod and food availability.

Levels of plasma oxytocin in male Peromyscus californicus were assessed across the reproductive cycle to provide a foundation for subsequent studies of the hormonal basis of paternal behavior and pair bonds. In Experiment 1, plasma oxytocin levels were significantly higher in expectant fathers than in virgin males or fathers. Plasma oxytocin increased in expectant fathers 1 day postcopulation and remained elevated for the first 15 days of gestation. Plasma oxytocin declined by Day 20 of gestation and oxytocin levels remained low in fathers throughout the lactational period. Oxytocin levels among expectant fathers did not differ between parental and nonparental males or between infanticidal and noninfanticidal males, suggesting that plasma oxytocin may not be involved in the prepartum onset of paternal behavior or the inhibition of infanticide. In Experiment 2, plasma oxytocin levels also did not differ between males that were parental or non-parental prepartum or postpartum. However, males separated from their mate and pups on the day of birth had elevated oxytocin levels on Day 3 postpartum compared to males that remained with their family, suggesting that disruption of the pair bond and/or absence of the young affects plasma oxytocin levels in males. This possibility remains to be determined.

The urinary profiles of adult female and male California mice were examined to determine the volatile compounds that may affect reproduction. The urinary volatiles identified by gas chromatography-mass spectrometry (GC-MS) include ketones, pyrazines, alkanes, nitrile, and aldehyde. None of volatile compounds was specific to males or females. The concentration of urinary volatiles in pregnant and lactating females was significantly higher than in virgin females. Male urinary volatile concentrations were similar to those of pregnant and lactating females. The GC profiles of both sexes were distinguished by a high percentage (36%) of pyrazine derivatives that were also in unusually high concentrations. These compounds may play a wide-ranging role in the control of reproduction in the California mouse.

The medial preoptic area (MPOA) is important in the control of maternal behavior in rodents, and it is sexually dimorphic. This study demonstrates that the MPOA of nonparental virgin male Peromyscus californicus (n = 10) is larger than that of virgin females (n = 9) because of a significantly greater number of neurons in the MPOA of virgin males. However, this sex difference in MPOA volume disappeared when males and females became parents. Soma size increased significantly when females became mothers. These data suggest that maternal behavior may require a structural change in the MPOA, whereas paternal responsivity, which is normally inhibited in virgin males, may require a change in neuronal activity. Furthermore, these results underscore the importance of reproductive status in examination of sexually dimorphic nuclear structures.

Preweanling rat pups do not display an aversion to a flavor conditioned stimulus (CS) paired with illness if the CS is presented during the act of suckling. In contrast, 20-day-old pups do form such a conditioned taste aversion while suckling (Martin & Alberts, 1979). The dissolution of the nursing-related "blockade" of toxiphobia correlates with the onset of solid food intake. Moreover, prevention of weaning prolongs the blockade; ingestive experience with solid food is necessary for the expression of nursing-related taste aversions in 26-day-old "food naive" pups (Gubernick & Alberts, 1984). The present experiments tested the possibility that premature weaning to solid food might accelerate the onset of nursing-related toxiphobia. Pups were weaned at 13 days of age and ingested only food and water. These prematurely weaned pups received taste aversion conditioning while suckling on Day 16, but showed no aversion to the CS flavor during a later food test. Thus, conditions that lead to early weaning (ingestion of solid food) do not accelerate the onset of taste aversions to mother's milk.

Mammalian mothers provide water to their young via milk. Rodent mothers reclaim much of this water by licking the anogenital areas of their pups, stimulating reflexive urination, and consuming the pups' urine. Male rodents do not provide milk (hence water) to the young, but in some species male parents may nevertheless lick their pups. We determined the amount of water transfer from pups to mothers and fathers in the biparental California mouse, Peromyscus californicus, by injecting 5-, 10-, 20-, and 30-day-old pups with tritiated water and measuring the radioactive label in maternal and paternal plasma after 24 hr of interaction with their litter. On Days 5 and 10 mothers obtained more pup urine than did fathers. Parents consumed equivalent amounts of pup urine on Days 20 and 30. Mothers engaged in more pup anogenital licking than did fathers, which accounted for the difference in pup urine consumption. Salt appetite controls in part, pup anogenital licking in lactating rats (Gubernick & Alberts, 1983). Salt appetite was not implicated in the modulation of anogenital licking in the California mouse because the mice failed to display a salt appetite. Licking of young and urine consumption are not dependent solely on the bidirectional exchange of water between the dam and her offspring.

During ontogenesis, altricial mammals advance through different ecological niches which require correspondingly different adaptive strategies. We view learning as an important feature of ontogenetic adaptations and consider the acquisition and expression of taste aversion learning during nursing within this framework. Fifteen-day-old preweanling rat pups fail to acquire conditioned taste aversions while nursing, whereas 20-day-old weanlings readily learn flavor aversions while suckling (Martin & Alberts, 1979). The developmental emergence of taste aversion learning while nursing coincides with reduction in maternal milk supply and the rat pup's transition to a solid food diet. We considered the ontogenetic transformation of learning while nursing as a feeding-related adaptive strategy of the weanling rat and tested two predictions derived from this view: (1) delayed weaning might postpone acquisition or expression of suckling-related taste aversions and (2) conditions that permit weaning (e.g., access to alternate food sources) might induce acquisition or expression of such taste aversions. Both predictions were confirmed.

Rat mothers lick the anogenital area of their young, stimulate reflexive urination, and ingest the urine. To quantify the transfer of body water from offspring to mother, we injected 5- to 30-day-old rat pups with tritiated water and the next day measured the radioactive label in maternal plasma. Rat dams reclaim about 16 ml of water/day from 5-day-old litters, 20 ml/day from 10-day-olds, and 40 ml/day from 15-day-olds. Urine consumption decreases to negligible amounts by Day 30. Time-lapse video recordings were used to measure maternal anogenital licking from Days 1-31 postpartum. Water transfer correlated with the developmental diminution of maternal anogenital licking. Maternal anogenital licking is controlled, in part, by the transfer of water from litter to dam and by the mother's salt appetite. Anogenital licking of pups was decreased after dams ingested a 0.15 M solution of NaCl but not after consumption of KCl, implicating a sodium specific mechanism. Licking of other regions of the pup's body was not affected. We discuss mother-infant interactions in terms of bidirectional exchanges of resources that constitute a "symbiotic" association.

Most knowledge of parent-offspring relations in mammals is derived from studies of mother-infant interactions. Male parental care has been less well studied. We explored maternal and paternal behavior of the California mouse, Peromyscus californicus. Six pairs of parents and their young were videotaped continuously for 12 hours/day, on alternate days from Days 1 to 31 postpartum. Males exhibit all parental activities and to the same extent as displayed by mothers, except lactation. Male parental behavior begins on the day of birth. Mothers and fathers spend substantial and equivalent amounts of time in the nest and in physical contact with pups throughout lactation. Males devote more time than females to licking pups, although females engage in more pup anogenital licking. Mothers nurse for at least 4 weeks, and fathers and mothers both build nests and carry young. The biparental care system of Peromyscus californicus affords an opportunity to develop a broader, more complete view of parent-offspring relations.

Rat dams provide water to their young via milk. Dams reclaim much of this water by licking the pups' anogenital areas, stimulating reflexive urination and consuming the pups' urine. Sensitized virgin rats, induced to act maternally do not provide water to pups, but they nevertheless lick them. To determine whether bidirectional transfer of water between the rat mother and her litter mediates maternal licking, water transfer from pups to sensitized virgins was compared with that to lactating dams. We used time-lapse video recordings to measure anogenital licking of pups. Sensitized virgins and lactating dams spent equivalent amounts of time licking the anogenital regions of test litters. We quantified the amount of water transferred from offspring to both virgins and dams by injecting pups with tritiated water and measuring the radioactive label in maternal plasma after interaction with a litter of 5-day-olds. Dams obtained more than twice as much urine from the litter in 4 hr than did the maternal virgins. Differences in the amount of water obtained from pups were due to differences in urine availability caused by the receipt of milk from the dams. When the dams' nipples were ligated, so that their pups received no milk, ligated dams and virgins consumed equivalent amounts of pup urine. Maternal licking and urine consumption are not dependent solely upon the bidirectional exchange of water between the dam and her offspring.

Relatively little is known about hormonal mechanisms underlying paternal behavior in mammals. Male California mice, Peromyscus californicus, display extensive parental care toward their young. Parental behavior of fathers, expectant fathers (males living with their pregnant partner), and virgin males was assessed in a 10-min test with a 1- to 3-day-old alien pup. Few virgin males acted parental (19%) compared to fathers one day postpartum (80%) and expectant fathers (56%). Plasma prolactin levels were significantly elevated in fathers 2 days postpartum compared to expectant fathers and virgin males. Paternal prolactin levels were similar to those of mothers. There were no differences between groups in levels of plasma testosterone. These data suggest, contrary to other reports, that prolactin is a likely correlate of paternal behavior in rodents.