Accounts of food sharing within natural populations of mammals have focused on transfers to offspring or transfers of food items that are difficult to obtain (such as meat). Five groups of socially monogamous owl monkeys (Aotus azarai azarai) in Formosa, Argentina were observed during 107 hr to determine the pattern of food sharing under natural conditions. There were a total of 42 social interactions involving food with food being transferred on eight occasions. Adult males transferred food to young more often than did adult females. All types of food that were readily obtained and eaten by all age/sex classes were transferred to young. Adult females also transferred food to their mates. This type of food sharing is very rare among animals and may have social benefits specific to monogamous mammals with paternal care.
Fatherhood in biparental mammals is accompanied by distinct neuroendocrine changes in males, involving some of the same hormones involved in maternal care. In the monogamous, biparental California mouse (Peromyscus californicus), paternal care has been linked to changes in the central and/or peripheral availability of oestrogen, progesterone, vasopressin and oxytocin, although it is not known whether these endocrine fluctuations are associated with changes in receptor availability in the brain. Thus, we compared mRNA expression of oestrogen receptor (ER)α, progesterone receptor (PR), vasopressin receptor (V1a) and oxytocin receptor (OTR) in brain regions implicated in paternal care [i.e. medial preoptic area (MPOA)], fear [i.e. medial amygdala (MeA)] and anxiety [i.e. bed nucleus of the stria terminalis (BNST)] between first-time fathers (n = 8) and age-matched virgin males (n = 7). Males from both reproductive conditions behaved paternally towards unrelated pups, whereas fathers showed significantly shorter latencies to behave paternally and less time investigating pups. Furthermore, fathers showed significantly lower PR, OTR and V1a receptor mRNA expression in the BNST compared to virgins. Fathers also showed a marginally significant (P = 0.07) reduction in progesterone receptor mRNA expression in the MPOA, although fatherhood was not associated with any other changes in receptor mRNA in the MPOA or MeA. The results of the present study indicate that behavioural and endocrine changes associated with the onset of fatherhood, and/or with cohabitation with a (breeding) female, are accompanied by changes in mRNA expression of hormone and neuropeptide receptors in the brain.
Social environment and parental state affect stress responses in mammals, but their impact may depend on the social and reproductive strategy of the species. The influences of cohabitation with a male or female conspecific, and the birth of offspring, on the physiological and endocrine responses to chronic variable stress were studied in the monogamous and biparental California mouse (Peromyscus californicus). Adult male California mice were housed either with a male cage mate (virgin males, VM), a female cage mate (pair-bonded males, PBM), or a female cage mate and their first newborn litter (new fathers, NF). VM, PBM and NF underwent a 7-day chronic variable stress paradigm (CVS, three stressors per day at semi-random times, n=7-8 per housing condition). Compared to control males (CON, n=6-7 per housing condition), CVS caused loss of body mass, increased basal plasma corticosterone concentrations, and increased basal expression of arginine vasopressin (AVP) mRNA in the paraventricular nucleus of the hypothalamus (PVN). These effects were independent of housing condition. Neither CVS nor housing condition altered novel-stressor-induced corticosterone release, spleen or testis mass, or basal expression of corticotropin-releasing hormone (CRH) mRNA in the PVN. Although CVS appeared to increase adrenal mass and reduce thymus mass specifically in NF, these effects were explained by the lower adrenal mass and higher thymus mass of NF compared to PBM and VM under control conditions. These results suggest that neither engaging in a pair bond nor becoming a father attenuates typical responses to CVS, but that fatherhood may provide a buffer against transient mild stressors (i.e., weighing and blood sampling in the control groups) in this monogamous and biparental rodent.
California mice Peromyscus californicus are a rodent species in which fathers provide extensive paternal care; however, behavioral responses of virgin males toward conspecific neonates vary from paternal behavior to tolerance to infanticide. Indirect evidence suggests that paternal responses might be influenced by social status potentially through increased stress and anxiety in subordinate males. To test this hypothesis, we housed 12 virgin male California mice in same-sex dyads on weaning and assessed their within-dyad subordinate or dominant status using food-competition and urine-marking tests. In addition, behavioral responses to an unrelated pup, expression of vasopressin (AVP) and corticotropin-releasing hormone (CRH) mRNA in the paraventricular hypothalamic nucleus (PVN), basal plasma levels of testosterone and corticosterone, and body mass were measured. Food-competition and urine-marking tests did not reveal strong or stable dominance-subordination relationships in male-male dyads. Latency to sniff a newborn pup was correlated negatively with urine marking in the center of a novel environment and positively with expression of AVP mRNA in the PVN. Because these three parameters are all associated with state anxiety in other rodent species, these results suggest that individual differences in paternal responsiveness may be influenced by individual differences in anxiety but not necessarily by social status in virgin male California mice.
Studies of biparental mammals demonstrate that males may undergo systematic changes in body mass as a consequence of changes in reproductive status; however, these studies typically have not teased apart effects of specific social and reproductive factors, such as cohabitation with a female per se, cohabitation with a breeding female specifically, and engagement in paternal care. We aimed to determine whether California mouse (Peromyscus californicus) fathers undergo systematic changes in body mass and if so, which specific social/reproductive factor(s) might contribute to these changes. We compared mean weekly body masses over a 5-week period in 1) males housed with another male vs. males housed with a non-reproductive (tubally ligated) female; 2) males housed with a tubally ligated female vs. males housed with a female that was undergoing her first pregnancy; and 3) experienced fathers housed with vs. without pups during their mate’s subsequent pregnancy. Body mass did not differ between males housed with another male and those housed with a non-reproductive female; however, males housed with a non-reproductive female were significantly heavier than those housed with a primiparous female. Among experienced fathers, those housed with pups from their previous litter underwent significant increases in body mass across their mates’ pregnancy, whereas fathers housed without pups did not. These results suggest that male body mass is reduced by cohabitation with a breeding (pregnant) female, but not by cohabitation with a non-reproductive female, and that increases in body mass across the mate’s pregnancy are associated with concurrent care of offspring rather than cohabitation with a pregnant female. Additional work is needed to determine the mechanisms and functional significance, if any, of these changes in male body mass with reproductive condition.
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.
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