Behavioral and endocrine consequences of heterosexual pair formation in squirrel monkeys

The South American squirrel monkey (Saimiri sciureus) typically lives in large social groups containing several individuals of all age/sex categories. When living in established heterosexual pairs, reproduction in this seasonally breeding primate is poor. We attempted to induce breeding activity in pair-housed monkeys by forming new heterosexual pairs just prior to the breeding season. Breeding readiness, as reflected in behavior and gonadal hormones, was induced in males, but not in females. Males also showed persistent increases in cortisol levels following formation of new heterosexual pairs; females did not. The results indicate that social stimulation provided by a single novel female is sufficient to enhance breeding readiness in male squirrel monkeys. Females, on the other hand, are apparently unresponsive to a single male whether novel or familiar; this may account for the poor reproductive success in squirrel monkeys housed in heterosexual pairs.     

Social interactions differentially affect reproductive and immune responses of Siberian hamsters

Social interactions can have pronounced effects on reproductive physiology and behavior in a wide range of species. Much less is known about the effects of social interactions on immunity. The goal of the present study was to test the effects of social interactions on both reproductive and immune responses in Siberian hamsters (Phodopus sungorus). Male and female hamsters were housed alone, in same-sex pairs or in mixed-sex pairs for 4 weeks. Animals were then immunized with the antigen keyhole limpet hemocyanin (KLH) and blood samples were drawn 5 days postinoculation. Reproductive tissue masses, testosterone, 17beta-estradiol and cortisol concentrations were measured and immunity was assessed by measuring serum anti-KLH IgM, and mitogen-stimulated splenocyte proliferation. Male hamsters housed with a female had increased testosterone and anti-KLH IgM and elevated splenocyte proliferation compared with males housed alone. Female hamsters housed in same-sex pairs had increased serum IgM compared with females housed with males. Cortisol was elevated in both sexes housed with male conspecifics compared with the other experimental groups. Serum estradiol concentrations did not differ among females in any group. Collectively, the results of the present study suggest that social interactions can alter reproductive responses, but that these changes appear unrelated to changes in immunity. In contrast, the presence of a male conspecific elicits social-stress-induced elevations in serum cortsiol in both males and females, which is generally immunosuppressive. These data support the notion of social-stress-induced suppression of immune humoral and cell-mediated immune responses.     

Male rank affects reproductive success and offspring performance in bank voles

Laboratory studies reveal that in several rodent species the females prefer dominant males as mating partners. Here we investigate the correlation between males' social rank and their reproductive success. Similar numbers of females mating with relatively more dominant or relatively more subordinate males produced a litter, and parturition took place 19-21 days after mating. Relatively more dominant males tended to sire more pups than did relatively more subordinates, but the mean number of offspring per litter did not differ significantly between the two groups. Significantly more pups fathered by relatively more dominant males survived to weaning than those sired by relatively more subordinate fathers. Dominance had a long-term effect on the reproductive activity of the offspring: their rate of sexual maturation was increased. In pups sired by a relatively more dominant father, the uteruses of females, and the testes and accessory sex glands of males, were significantly heavier than those of offspring born to relatively more subordinate males. Our results suggest that social rank is an important determinant of the reproductive success of bank vole males.     

Social dominance and reproductive success in pregnant and lactating golden hamsters (Mesocricetus auratus) under seminatural conditions

Pairs of female hamsters were acclimated to seminatural enclosures and permitted to interact for brief periods on days 12-14 of gestation or on days 2-4 of lactation. In one experimental paradigm, food was provided in excess of the daily requirements while in a second, food rations were restricted. Control females were similarly housed and fed but were not exposed to another animal. Paired females readily established dominant-subordinate relationships. Dominant females successfully removed food from the subordinate females and, as a result, accumulated larger food hoards. Subordinate females gave birth to fewer pups than either dominant or subordinate animals when social interactions occurred late in pregnancy and maintained smaller litters when interactions occurred during lactation. Reductions in the fecundity of subordinate females were more pronounced when the food ration was restricted. Under ad lib feeding conditions dominant females also maintained fewer young than control animals, but when food was restricted they were more successful than the control group. Subordinate females successfully defended their burrows against intrusions by dominant animals; maternal cannibalism accounted for most reductions in litter size. These results suggest that a defensible burrow and the acquisition of a food hoard are essential for successful reproduction in this species.     

Seasonal changes in chronic social interactions and physiological states in female rat-like hamsters (Tscheskia triton)

We examined the behavioral characteristics and physiological states related to solitary lifestyle and dominant-subordinate relationships in female rat-like hamsters (Tscheskia triton), formerly known as Cricetulus triton. Wild adult hamsters were captured and caged singly in the laboratory during the non-breeding and breeding seasons. The experimental hamsters were subjected to 5 min staged dyadic encounters every day for 28 consecutive days by pairing two unfamiliar and weight matched females in a neutral arena. Aggressive behavior, defense and flank marking were quantified everyday within the first week and once each week during the last 3 weeks. Animals were then autopsied and their physiological and reproductive state assessed. Our results suggested that dominant-subordinate relationships could be established especially in non-breeding conditions, where the dominant displayed higher aggression and flank marking, and lower defense than its opponent. The breeding females followed this pattern except there was no difference in aggressive behavior, between the partners. The repeated encounters did not appear to reduce aggression or lead to amiable behavior or bonding. At the end of the experiment breeding females exhibited higher levels of serum estradiol, progesterone and corticosterone than non-breeding females. Both dominant and subordinate females in non-breeding condition had atrophied ovaries and uteri, whereas both dominant and subordinate females in breeding condition had hypertrophied ovaries and uteri. Non-breeding females possessed heavier and thicker flank glands than breeding females did. Dominant females displayed longer or thicker flank glands than subordinate did. Thus, our data suggest that the behavioral traits observed in our experiment support the solitary lifestyle of adult female rat-like hamsters and physiological state show some differences between social ranks or in both seasons.     

Effects of siblings on reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

Mongolian gerbils living with their natal families undergo delayed reproductive maturation while helping to rear their younger siblings, whereas those housed away from their natal families may mature earlier but often respond aggressively to unfamiliar pups. We tested whether cohabitation with pups contributes to reproductive suppression and inhibition of infanticidal behavior, using young males and females housed with (1) their parents and younger siblings (pups), (2) parents without pups, (3) mixed-sex littermate groups, or (4) mixed-sex groups of unrelated peers. Maturation in males was inhibited by cohabitation with the parents, while maturation in females was further suppressed in the presence of pups. Males in all housing conditions showed little aggression towards unfamiliar pups, whereas females were usually infanticidal unless housed with pups. Aggression toward pups was especially pronounced in females that were pregnant or undergoing ovulatory cycles. Thus, cohabitation with younger siblings may intensify reproductive suppression and inhibit infanticidal behavior in female gerbils, whereas male gerbils exhibit parentally induced reproductive suppression and low rates of infanticide even in the absence of younger siblings.     

Split circadian rhythms of female Syrian hamsters and their offspring

In several mammalian species, circadian pacemakers of breeding females synchronize the developing clocks of offspring by as of yet unspecified mechanisms. The present study assessed whether maternal communication of circadian rhythms extends beyond setting pacemaker phase to include transfer of a fundamental reorganization of component circadian oscillators from dams to pups. In Experiment 1, a regimen of daily novel wheelrunning previously demonstrated to split activity rhythms of adult male hamsters into two discrete components was shown to similarly reorganize female hamster rhythms. In Experiment 2, females split by this method and unsplit controls exposed to similar light environments were mated with males. Split and unsplit females were equally fecund, but the former weaned pups of lower body weight. After weaning into running wheel cages, offspring of split dams were more likely to exhibit split activity rhythms than were offspring of unsplit females. Among pups not categorized as split, moreover, maternal entrainment nonetheless influenced distribution of pup activity across the 24-h cycle. Entrainment patterns of split and unsplit pups resembled those of adults. Thus, split and unsplit hamster dams provide different entraining signals to their developing offspring. The influence of maternal rhythms extends beyond entraining phase to alter interactions between component circadian oscillators that underlie split activity bouts. Maternal effects did not persist beyond the second week postweaning in split or unsplit hamsters, however, and rhythms of many split pups later joined. Thus, the maternal influence on the pup's circadian pacemaker may be transient.     

Activity and reproductive state in the hamster: independent control by social stimuli and a circadian pacemaker

Entrainment of circadian rhythms by social communication between male and female Syrian hamsters (Mesocricetus auratus) was tested by recording the wheel-running activity of pairs kept in the same cage but separated by a wire mesh barrier. Before pairing, males and females were synchronized to light/dark cycles that were 180 degrees out of phase, and at the time of pairing the hamsters were placed into constant darkness (DD). The activity rhythms of males and females housed in a cage alone (isolated) were also recorded. The freerunning periods of paired and isolated hamsters were not different over six weeks in DD, and no phase-shifts of the paired animals' rhythms were seen, indicating that the close proximity of a hamster of the opposite sex had no effect on the timing of the other's activity/rest rhythm. This was not due to a lack of communication between the paired males and females. Males showed four-day cycles in the amount and distribution of activity which corresponded to the estrous cycle of the female, and regression of the reproductive system which occurred in the isolated hamsters was delayed in both the paired males and females. Despite the fact that locomotor activity and reproduction are each regulated in part by a circadian pacemaker, social stimuli can affect both of these without influencing the circadian pacemaker that underlies the activity/rest rhythm.     

Litter deficits of socially stressed and low status hamster dams

The effects of maternal social stress, induced by pairing pregnant females, and social status, measured by agonistic behavior within pairs, on pup development was investigated in hamsters. Using litters from untreated first pregnancies as a control, 40 dams were housed either alone or paired with another dam during their second pregnancy. Within a pair, the dam with more aggressive and fewer defensive responses than the other was considered dominant. Compared to their first unpaired litters, second litters of paired dams were smaller in number. Comparisons among second litters showed that paired dams, especially submissive dams, had fewer pups than unpaired dams. It was concluded that both maternal social stress and low status increase intrauterine mortality.     

Induction of obesity by group housing in female Syrian hamsters

We examined the effects of group housing on body weight in adult female Syrian hamsters. Over a 10-week period, female hamsters housed in groups of 5 per cage increased their body weight by 61% compared with an 18% increase in body weight for female hamsters housed individually. The divergence in body weight between females housed in groups and females housed individually was evident as early as 2 weeks after the start of the experiment. At the end of the 10 weeks, group-housed females were significantly longer, had a higher percentage of body fat, and larger adrenal glands compared with these measures from individually housed hamsters. These results demonstrate that housing conditions can have a powerful effect on body weight and body composition in female Syrian hamsters. These effects are discussed in the context of social stress mediating obesity in Syrian hamsters, and offer the possibility for a socially based animal model of obesity.     

An immunohistochemical study of the gonadotrophin-releasing hormone 1 system in solitary Cape mole-rats, Georychus capensis, and social Natal mole-rats, Cryptomys hottentotus natalensis

Mole-rat species within the family Bathyergidae exhibit a wide range of reproductive strategies and social systems. Various forms of reproductive suppression are displayed within this family: in the solitary species, breeding is suspended for part of the year and in the social species, reproduction is suppressed in subordinate animals. This study investigated the gonadotrophin-releasing hormone 1 (GnHR-1) systems of breeding and non-breeding solitary Cape mole-rats and social Natal mole-rats for possible inter- and/or intra-species differences. In both species, GnRH-1 cell bodies are predominantly in the medial septum region of the diagonal band or the preoptic area, with relatively few in the mediobasal hypothalamus; a dense concentration of GnRH-1-immunoreactive (ir) processes is present in the region of the organum vasculosum of the lamina terminalis. In Cape mole-rats, GnRH-1-ir processes are particularly dense within the lateral margins of the median eminence, which is enfolded by a large pars tuberalis of the pituitary gland. Natal mole-rats display GnRH-1-ir processes across the breadth of the median eminence, which is abutted by a relatively small pars tuberalis. There are more GnRH-1-ir cell bodies in Natal mole-rats than in Cape mole-rats (∼720 vs. ∼420). No significant differences were found in the number, distribution or size of GnRH-1-ir cell bodies according to season in Cape mole-rats or according to reproductive status or sex in Natal mole-rats. In female and male Natal mole-rats, GnRH-1-immunoreactivity in the median eminence is less dense in the reproductive animals; no such difference was found in Cape mole-rats between the breeding and non-breeding seasons. These immunohistochemical results are discussed in the light of earlier studies which identified no functional neuroendocrine impediments underlying regulated reproduction in either Cape or Natal mole-rats. The cumulative findings suggest that the principal factors determining seasonal or socially induced suppression of reproduction in these species are behavioral rather than neuroendocrine.     

A Longitudinal Study of the Sociosexual Dynamics in a Captive Family Group of Wolves: The University of Connecticut Wolf Project

An interest in the role of the social environment on the evolution of behavior led Professor Benson Ginsburg to studies of wolf social behavior. He initiated the University of Connecticut wolf project with a family group of wolves housed in a protected enclosure in an isolated area of campus. One aim of this project was to conduct a longitudinal study of a family group of wolves in order to understand the proximate behavioral mechanisms underlying mating dynamics with a degree of control and opportunistic observation that could not be achieved through field studies. The development of social relationships and the dynamics of mating were observed for 9 years. As in nature, agonistic relationships strongly influenced reproductive success, successful breeding was limited to a single pair each season, and the behavioral dynamics included status transitions with breeder rotations. Our work, when combined with the results of other captive wolf studies, has contributed valuable information to the general understanding of wolf social behavior, especially regarding the proximate behavior patterns underlying group social interactions and reproduction. This understanding has broadened perspectives on the dynamic interplay between social behavior and evolutionary processes.     

The reproductive success of the parasitic bat fly Basilia nana (Diptera: Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein’s bat (Myotis bechsteinii)

We studied the reproductive ecology of the bat fly Basilia nana on free-ranging colonial female and solitary male Bechstein’s bats (Myotis bechsteinii) during one reproductive season. The reproduction of B. nana took place from April to September, and the production of puparia in bat roosts was high. The metamorphosis of the flies took a minimum of 30 days, and at least 86% of the puparia metamorphosed successfully. However, only about 30% of flies from puparia deposited in female roosts and 57% of flies from puparia deposited in male roosts emerged in the presence of Bechstein’s bats and were thus able to survive. The significantly higher emergence success of bat flies in male roosts was caused by the higher roost fidelity of the solitary males compared with the social females. Our results indicate that bats can control the reproductive success of bat flies by switching and selecting roosts.     

Same-sex social behavior in meadow voles: Multiple and rapid formation of attachments

Adult meadow voles (Microtus pennsylvanicus) are solitary in the spring-summer reproductive season, but during winter months, females and males are socially tolerant and aggregate in groups. This behavioral difference is triggered by day length: female meadow voles housed in short, winter-like day lengths form same-sex partner preferences, whereas those housed in long, summer-like day lengths are less social. The present study demonstrates that same-sex social attachments in short day lengths are not exclusive; females formed concurrent attachments with more than one individual, and with non-kin as well as siblings. Partner preferences between females were established within one day of cohousing and did not intensify with greater durations of cohabitation. Males also formed same-sex social attachments, but unlike female affiliative behavior, male partner preferences were not significantly affected by day length. These data are discussed in the context of field behavior and the physiological mechanisms supporting social behavior in voles.     

Effects of weasel odor on behavior and physiology of two hamster species

This study examined the behavioral and physiological effects of long-term exposure to overdose of aversive odor (predator odor) in two species of hamsters. About 0.05 mg of anal gland secretions of Siberian weasels (Mustela sibirica) was smeared at the oronasal groove of wild male ratlike hamsters (Cricetulus triton) (natural prey) and laboratory golden hamsters (Mesocricetus auratus) once every day for 4 weeks. After 28 days, the experimental groups of both hamster species displayed higher cortisol level, larger adrenal gland (in ratlike hamsters only), smaller thymus and flank gland, and lower aggression level than the conspecific control group (presented with water). Thus, the long-term presence of overdose of the anal gland secretion of the Siberian weasel could lower the aggression and social rank and suppress the immunity in the hamsters. The reproductive conditions of these prey species, however, seemed not to be affected. In addition, the similarities in the behavioral and physiological responses to the predator odor between the two species of hamsters showed that the responses to predator odor might be innate.     

Prolactin levels in paternal striped mouse (Rhabdomys pumilio) fathers

Paternal behavior is associated with an increase in prolactin levels in fish, birds and mammals, including rodents. The striped mouse (Rhabdomys pumilio) from southern Africa shows highly developed paternal care. We investigated whether striped mouse fathers have higher prolactin levels than nonfathers, and whether there is a relationship between tactile stimulation with pups and prolactin secretion in fathers. We measured serum prolactin in 42 male striped mice assigned to one of four different experimental groups (single males, paired males, fathers housed with mother and pups, and fathers separated from their family by a wire-mesh partition). Our results revealed no increases in prolactin levels in fathers, and fathers with tactile contact with pups did not have higher prolactin levels than the fathers that were prevented from making tactile contact with pups. In contrast, experienced males had higher prolactin levels than inexperienced males. Male striped mice are polygynous in nature, living in groups, with three breeding females, and are permanently associated with pups during the breeding season. In a field study, males had higher prolactin levels during the breeding season than during the nonbreeding season. Thus, prolactin secretion in the polygynous striped mouse might be regulated by environmental stimuli, whereas social stimuli might be important for monogamous species. This is the first study to demonstrate seasonal changes in prolactin levels in a free-living male mammal.     

Breeding readiness in squirrel monkeys: female-primed females are triggered by males

The South American squirrel monkey (Saimiri) shows pronounced annual variations in reproductive activity. We investigated the contribution of social stimulation to breeding readiness, as reflected in behavior and gonadal hormones. A previous study indicated that formation of new heterosexual pairs can induce breeding readiness in males, but not in females. In the present study we examined the response of individually housed females to the formation of triads of unacquainted females and, subsequently, the response of these triads to the introduction of a single male. The formation of the all-female group was accompanied by a marked reduction in basal cortisol levels. Introduction of a male to such a group promptly induced breeding readiness in the females, as indicated by increased gonadal hormone production and cyclic variation in estrogen and progesterone levels. The contrasting responses of group-living or single females to a new male suggest that at least two processes are involved in the induction of breeding readiness by group formation in females. One is a "priming" effect resulting from interfemale stimulation: the other is a "triggering" effect resulting from the presence of a male.     

Olfactory experience and the development of odor preference and vaginal marking in female Syrian hamsters

Rodent reproductive behavior relies heavily on odor processing, and evidence suggests that many odor-guided sexual behaviors are shaped by prior experience. We sought to determine if exposure to male odors during development is required for the adult expression of proceptive sexual behavior toward male odors in female Syrian hamsters. Exposure to male odors was restricted in na?ve subjects by removing all male siblings from the litter at three to five days of age. Control litters were also culled, but included equal numbers of male and female pups. As adults, na?ve females displayed investigatory preferences toward male odors in a Y-maze that were comparable to control females; this preference was observed whether contact with the odor stimuli was prevented of allowed. In contrast, na?ve females vaginal scent-marked equally toward male and female volatile odors, suggesting an inability to target behavior toward sexually relevant odors. However, na?ve females marked preferentially toward male odors when allowed to contact the odor stimuli. These results provide evidence for the experience-dependent development of vaginal marking behavior toward volatile components of sexual odors. Furthermore, they suggest that distinct mechanisms regulate the development of odor preferences and vaginal marking behavior in this species.     

Acceleration of reproductive development in female Djungarian hamsters by adult males

Housing young female Djungarian hamsters (Phodopus campbelli) with an adult male accelerates uterine and ovarian development and there is a strong relationship between uterine weight and ovarian measures (e.g., follicular size). Uterine weights of females housed with an adult male for 10 days following weaning are comparable to values from females housed alone for 25 days. Removal of endogenous androgens by castration eliminated the capacity of adult males to accelerate reproductive development in young females and treatment of castrated males with exogenous androgens maintained the production of the acceleratory chemosignal. When adult male urine and ventral gland sebum were examined as possible sources for the acceleratory chemosignal, only male urine had an acceleratory effect on reproductive development. Thus, female Djungarian hamsters respond with accelerated reproductive development to androgen-dependent chemosignals in the urine of adult males. These mechanisms are similar to those found in several other rodents but contrast with the lack of such effects in the golden hamster (Mesocricetus auratus).     

Early fitness consequences and hormonal correlates of parental behaviour in the social rodent, Octodon degus

Males are expected to assist their mates whenever this behaviour raises survival of offspring with little expense in terms of mating opportunities. At a more proximate level, cortisol and testosterone hormones seem involved in the expression of parental care in mammals. We examined the consequences to postnatal offspring development and survival of the males' presence in the social rodent, Octodon degus. Offspring quality and quantity, and maternal condition of females were contrasted among females rearing their litters in the presence of the sire, females breeding in the presence of a non-breeding female, and females breeding solitarily. We related these differences to variation in parental behaviour and plasma levels of testosterone and cortisol. Twenty two females and their litters were studied under constant conditions of adult density, nest availability, food availability, and breeding experience. Males huddled over and groomed offspring. However, neither the number nor the mass of pups from dams that nested with the sire differed from those recorded to breeding females that nested with a non-breeding female and females that nested solitarily. Body weight loss and associated levels of plasma cortisol in dams nesting with the sire were similar to those of solitary females, but higher than mothers nesting with a non-breeding female. Thus, male care had no consequences to offspring, and seemed detrimental to breeding females. Circulating levels of cortisol and total testosterone were either poor (mothers) or no (fathers, non-breeding females) predictors of parental care.