Short-day increases in aggression are independent of circulating gonadal steroids in female Siberian hamsters (Phodopus sungorus)

Among the suite of adaptations displayed by seasonally-breeding rodents, individuals of most species display reproductive regression and concomitant decreases in gonadal steroids during the winter. In addition, some species display increased aggression in short "winter-like" days compared with long "summer-like" day lengths. For example, male Syrian and Siberian hamsters held in short days express heightened levels of aggression that are independent of gonadal steroids. Virtually nothing is known, however, regarding seasonal aggression in female Siberian hamsters (Phodopus sungorus). Studies were undertaken to determine female levels of aggression in long and short days as well as the role of gonadal steroids in mediating this behavior. In Experiment 1, females were housed in long or short days for 10 weeks and resident-intruder aggression was assessed. Prior to testing, estrous cycle stages were determined by vaginal cytology and females were tested during both Diestrus I and Proestrus. In Experiment 2, hormone levels were experimentally manipulated; long-day females were ovariectomized (OVx) or given sham surgeries whereas short-day females were implanted with capsules containing 17beta-estradiol (E(2)) or Progesterone (P). In Experiment 3, both long- and short-day females were ovariectomized and implanted with either an exogenous E(2) or blank capsule, or given a sham surgery. Short-day hamsters displayed increased aggression relative to long-day females. Aggression was not affected by estrous stage. There was no difference in aggression between long-day OVx and sham animals. Furthermore, neither exogenous E(2) nor P had any significant effect on aggression. These results support previous findings of increased non-breeding aggression and suggest that short-day aggression is not likely mediated by circulating levels of gonadal steroids. These results also suggest that the endocrine regulation of seasonal aggression may be similar between the sexes.     

Short-day increases in aggression are inversely related to circulating testosterone concentrations in male Siberian hamsters (Phodopus sungorus)

Many nontropical rodent species display seasonal changes in both physiology and behavior that occur primarily in response to changes in photoperiod. Short-day reductions in reproduction are due, in part, to reductions in gonadal steroid hormones. In addition, gonadal steroids, primarily testosterone (T), have been implicated in aggression in many mammalian species. Some species, however, display increased aggression in short days despite basal circulating concentrations of T. The goal of the present studies was to test the effects of photoperiod on aggression in male Siberian hamsters (Phodopus sungorus) and to determine the role of T in mediating photoperiodic changes in aggression. In Experiment 1, hamsters were housed in long and short days for either 10 or 20 weeks and aggression was determined using a resident-intruder model. Hamsters housed in short days for 10 weeks underwent gonadal regression and displayed increased aggression compared to long-day-housed animals. Prolonged maintenance in short days (i.e., 20 weeks), however, led to gonadal recrudescence and reduced aggression. In Experiment 2, hamsters were housed in long and short days for 10 weeks. Half of the short-day-housed animals were implanted with capsules containing T whereas the remaining animals received empty capsules. In addition, half of the long-day-housed animals were castrated whereas the remaining animals received sham surgeries. Short-day control hamsters displayed increased aggression compared to either castrated or intact long-day-housed animals. Short-day-housed T treated hamsters, however, did not differ in aggression from long-day-housed animals. Collectively, these results confirm previous findings of increased aggression in short-day-housed hamsters and suggest that short-day-induced increases in aggression are inversely related to gonadal steroid hormones.     

Metabolic stress suppresses humoral immune function in long-day,but not short-day,Siberian hamsters (<Emphasis Type="Italic">Phodopus sungorus</Emphasis>)

Individuals of many species experience marked seasonal variation in environmental conditions and must adapt to potentially large fluctuations in energy availability and expenditure. Seasonal changes in immunity have likely evolved as an adaptive mechanism to cope with seasonal stressors. In addition, these changes may be constrained by seasonal fluctuations in energy availability. The goal of this study was to assess the role of energetic trade-offs associated with seasonal variation in immunity. In addition to body fat stores, metabolic fuels (e.g., glucose) may affect immune function in seasonally breeding rodents. In this study we experimentally reduced energy availability via injections of the metabolic inhibitor 2-deoxy-d-glucose (2-DG) in long- and short-day housed Siberian hamsters (Phodopus sungorus) and then examined antigen-specific antibody production. Metabolic stress decreased antibody response compared with control animals in long days. In contrast, no difference was observed between treatment groups in short days. These data suggest that reductions in energy availability suppress immunity and short days buffer organisms against glucoprivation-induced immunosuppression.     

Chemosensory stimulation of luteinizing hormone secretion in male Siberian hamsters (Phodopus sungorus)

Male Siberian hamsters (Phodopus sungorus) housed in long days (LD), but not short days (SD) release luteinizing hormone (LH) when exposed to females. This study examined whether this response is specific to a female and identifies the source of a stimulus that induces LH release. Serum concentrations of LH, testosterone (T), follicle stimulating hormone (FSH), and cortisol were examined in all experiments. T concentrations mirrored the LH response; FSH and cortisol were unchanged in response to all stimuli. Exposure to an LD female, irrespective of her reproductive status, but not an SD female, elicited LH release. Exposure to another male did not trigger LH release. Males released LH when allowed physical contact with an anesthetized female, but not when separated from a normally active female, suggesting that tactile or nonvolatile chemosensory stimuli elicit LH release. Urine and secretions collected from the vagina as well as oral, midventral, perineal, and rectal glands, elicited marked behavioral responses in male P. sungorus. Despite these behavioral responses, only feces from females elicited LH release in males. Males released LH in response to feces extracted from the rectum and to cotton swabs that had been rubbed against the rectal mucosa, suggesting that a component of rectal secretions may trigger LH release in male Siberian hamsters. Taken together, these data and previous data from our laboratory indicate that both the production of and the response to a pheromone that triggers the selective release of LH is regulated by day length.     

Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters (Phodopus sungorus)

Differential allocation of energy to reproduction versus host defense is assumed to drive the seasonal antiphase relation between peak reproductive function and immunocompetence; however, evidence supporting this assumption is only correlational. These experiments tested whether photoperiod affects immune responses to antigens in peripubertal Siberian hamsters, whether such activation of the immune system exacts energetic and reproductive costs, and whether such costs vary seasonally. Male Siberian hamsters were raised from birth in long (LD) or short days (SD), which respectively initiate or inhibit the onset of puberty. To elicit a specific immune response, hamsters were injected with a novel antigen (keyhole limpet hemocyanin [KLH]) as juveniles. Reproductive development was attenuated and body temperature was elevated in LD hamsters relative to saline-injected control animals. In contrast, KLH treatments affected neither thermoregulation nor reproductive development in photoinhibited SD hamsters. In experiment 2, juvenile male hamsters were challenged with bacterial lipopolysaccharide (LPS) in order to elicit an innate immune response. Febrile and anorexic responses to LPS were greater in reproductively stimulated LD hamsters relative to reproductively inhibited SD hamsters. LPS treatments attenuated somatic and testicular development in LD hamsters, but did not significantly affect circulating testosterone concentrations. In contrast, LPS treatments were without effect on somatic and reproductive development in SD hamsters. These experiments indicate that photoperiod affects antigen-specific antibody production, febrile responses to LPS, and sickness behaviors in juvenile Siberian hamsters, and that peripubertal activation of the immune system exacts energetic and metabolic costs that can diminish the magnitude of somatic and reproductive maturation in LD. The data also underscore the importance of seasonally dependent life history factors in assessing physiological tradeoffs.     

注射胸腺依赖和非胸腺依赖抗原雄性黑线毛足鼠的内分泌状态和气味吸引力

作者研究了胸腺依赖抗原 (SRBC) (羊红血细胞 ,sheepredbloodcells ,SRBC)和非胸腺依赖抗原 (细菌脂多糖 ,lipopolysaccharide ,LPS)的免疫活化对黑线毛足鼠气味信号和内分泌状态的影响。成年雄鼠注射SRBS5天后 ,其气味的性吸引力下降 ,这种结果伴随着粪便中睾酮含量的下降。SRBC处理后 ,雄性气味吸引力降低 ,这在体液免疫反应低的雄性个体中最明显。与SRBC的作用相反 ,注射LPS的雄性个体的气味吸引力增加 ,成熟雌性个体用于嗅闻嗅觉刺激上的时间差异与经LPS和盐处理过的雄鼠的粪便中睾酮浓度的差异呈正相关。作者讨论了这两种相反的嗅觉效应的适应性意义     

Social cues attenuate photoresponsiveness of the male reproductive system in Siberian hamsters (Phodopus sungorus)

Transfer of adult Siberian hamsters (Phodopus sungorus) from long (16 h light and 8 h dark, 16L:8D) to short (8L:16D) daily photoperiods induces an involution of the gonads and a cessation of reproductive behavior 8 to 10 weeks later. However, when male and female long-day hamsters were paired on transfer to short photoperiods, the males' gonads did not undergo the typical short-day response. Similarly, when male long-day hamsters were paired with refractory females (i.e., females housed in short photoperiods for at least 28 weeks so that they became unresponsive to short photoperiods), the response of the males' reproductive system to short photoperiods also was attenuated. Thus, social cues can override or delay the effects of photoperiod on the testes of this species. These results suggest that the inhibitory effects of long durations of melatonin secretion (in response to short photoperiods) on the male hypothalamic-pituitary-gonadal axis may be attenuated by social cues such as contact with the opposite sex.     

Perinatal photoperiod organizes adult immune responses in Siberian hamsters (Phodopus sungorus)

Individuals of many nontropical rodent species display reproductive, immunological, and somatic responses to day length. In general, short day (SD) lengths inhibit reproduction and enhance immune function in the laboratory when all other conditions are held constant. Most studies to date have focused on seasonal variation in immune function in adulthood. However, perinatal photoperiods also communicate critical day length information and serve to establish a developmental trajectory appropriate for the time of year. Nontropical rodents born early in the breeding season undergo rapid reproductive development, presumably to promote mating success during their first reproductive season. Rodents born late in the breeding season suspend somatic growth and puberty until the following vernal breeding season. We tested the hypothesis that perinatal day lengths have similar enduring effects on the immune system of rodents. Siberian hamsters (Phodopus sungorus) were maintained prenatally and until weaning (21 days) in either SDs (8 h light:16 h dark) or long days (LD) (16 h light:8 h dark), then they were weaned into either the opposite photoperiod or maintained in their natal photoperiod, forming four groups (LD-LD, LD-SD, SD-LD, and SD-SD). After 8-wk in these conditions, cell-mediated immune activity was compared among groups. SD-SD hamsters of both sexes enhanced immune function relative to all other groups. The reproductive effects of perinatal photoperiod were not evident by the end of the experiment; circulating testosterone and cortisol sampled at the end of the experiment reflected the postweaning, but not the perinatal photoperiod. This experiment demonstrates long-lasting organizational effects of perinatal photoperiod on the rodent immune system and indicates that photoperiod-induced changes in the immune system are dissociable from changes in the reproductive system.     

Photoperiod-related changes in hormonal and immune status of male Siberian hamsters,Phodopus sungorus

Previously we have demonstrated that in Siberian hamsters some immune measures, especially the development of experimentally evoked peritonitis, varied in a photoperiod- and gender-dependent manner. The aim of the present study was to investigate whether the photoperiod-related differences in the activity of inflammation-involved immune cells are in this species attributed to the changes in the pineal gland function and/or hormonal status. Male hamsters housed in short day (SD), compared with those from long day (LD) conditions, exhibited significantly reduced plasma testosterone concentration and elevated cortisol and melatonin levels, the latter resulting from increased activity of hydroxyindole-O-methyltransferase (HIOMT). In LD hamsters but not in those from SD, an intraperitoneal (i.p.) injection of zymosan evoked a well-pronounced peritonitis expressed by increased free radical (ROS) production by peritoneal leukocytes (PTLs) stimulated in vitro with PMA. ROS production by these cells was additionally stimulated by both in vivo and in vitro treatment with melatonin and the latter was partially reversed by melatonin receptor antagonist luzindole. To conclude, in Siberian hamsters melatonin seems to exert rather immunostimulatory than anti-inflammatory effect, therefore other mechanisms, e.g. immunosuppressive effect of glucocorticoids, may underlay the compromised immune status observed in SD in this species.     

Effects of wheel running on photoperiodic responses of Djungarian hamsters (Phodopus sungorus)

Djungarian hamsters (Phodopus sungorus) were exposed to artificial short days either with access to a running wheel (RW) or without. Within 6 weeks RW hamsters considerably increased their body mass, whereas controls showed the typical body mass reduction. Estimation of paired testis weights indicated a decelerated testis regression in RW hamsters. Subsequent locking of RWs for 9 weeks led to a decline in body mass of RW animals in parallel to controls. Daily torpor was almost completely missing in hamsters with initially unlocked wheels. During the final phase when RWs were again unlocked (3 weeks), body mass of exercising hamsters increased again, while controls reached the nadir in body mass. In comparison to equiponderate long-day (LD) controls the relative liver weight of RW hamsters was significantly increased unlike the relative heart weight. However, the latter tended to be higher than in sedentary LD hamsters. A growth-stimulating effect of wheel running was proven by elongated femora in exercising short-day (SD) hamsters compared to SD controls and suggested by exercise-induced elevation of body mass in a further experiment under continuous LD conditions, indicating a growth-promoting effect of wheel running independent from the photoperiod.     

Genetic and environmental influences on short-day responsiveness in Siberian hamsters (Phodopus sungorus)

Siberian hamsters are photoperiodic rodents that typically exhibit several physiological changes when exposed to a short-day photoperiod. However, development of the winter phenotype in short days is largely conditional on prior photoperiod history: Hamsters that have been reared in an exceptionally long day length (18 L) do not usually exhibit the winter phenotype after transfer to short days, whereas animals reared under "moderately" long days (16 L) are more variable in responsiveness to subsequent short-day exposure, with 20% to 30% generally failing to exhibit winter-type responses. Hamsters reared exclusively in an "intermediate" day length (14 L) are almost uniformly responsive to short photoperiod. In the present study, the authors examine the influence of photoperiod history on short-day responsiveness in a breeding line of hamsters that has been subjected to artificial selection for resistance to the effects of short days. The results demonstrate that photoperiod history is an important determinant of short-day responsiveness in both random-bred (UNS) hamsters and animals artificially selected and bred for nonresponsiveness to short photoperiod (PNR). The PNR hamsters have a reduced requirement for long-day exposure to evoke a state of unresponsiveness to short days. The results are discussed in relation to possible significance for the origin of population and species differences in photoperiod responsiveness.     

Possible mechanisms of weight loss of Siberian hamsters (Phodopus sungorus sungorus) exposed to short photoperiod

Several weeks of short day photoperiod (SD) exposure promote a dramatic decrease of white adipose tissue (WAT) mass in Siberian hamsters(Phodopus sungorus sungorus). This slimming effect is accompanied by changes in the adipocyte responsiveness to adrenergic stimulation that are still under debate. We investigated whether possible changes in the antilipolytic responses, and/or lipogenic activities could be involved in such lipid deposition/mobilisation imbalance. Male Siberian hamsters were exposed for 11 weeks to SD or long day photoperiod and basal or stimulated lipolytic and lipogenic activities were measured on white adipocytes. As expected, the body mass of SD-animals was decreased. Besides a slight reduction in the basal lipolysis and in the maximal response to dibutyryl-cAMP, the responses to adrenergic and non-adrenergic lipolytic agents (forskolin, adenosine deaminase) were similar in both groups. Fat mass loss was likely not resulting from changes in the lipolytic responses of adipocytes to biogenic amines (e.g. octopamine), which were unaltered, or to a direct lipolytic stimulation by melatonin or histamine, which were inactive. Antilipolytic responses to insulin or tyramine were slightly decreased in SD-adipocytes. Basal or insulin-stimulated lipid accumulation in WAT, measured by glucose incorporation into lipids, did not change after SD-exposure. However, a significant decrease in the lipoprotein lipase activity was observed in the WAT of SDanimals. Despite the observed changes, the weight loss of SD-exposed Siberian hamsters was likely not resulting only from impaired antilipolytic orde novo lipogenic activities in white adipocytes, but either from other dramatic changes occurring during seasonal photoperiod-sensitive body weight regulation.     

Photoperiodic regulation of adrenal hormone secretion and aggression in female Syrian hamsters

Seasonal changes in the length of the daily photoperiod induce significant changes in social behavior. Hamsters housed in winter-like short photoperiods (SP) can express significantly higher levels of aggression than hamsters housed in long photoperiods (LP) that mimic summer. The mechanisms responsible for increasing aggressiveness in SP-exposed female hamsters are not well understood but may involve seasonal changes in the endocrine system. In experiment 1, the effects of SP exposure on the circulating levels of three adrenal hormones were determined. Short photoperiod exposure was found to significantly depress the circulating levels of cortisol and the adrenal androgen dehydropiandrosterone (DHEA) but significantly increased the circulating levels of the sulfated form of DHEA, DHEAS. Experiment 2 examined the effects of gonadal hormones on several different measures of aggression including its intensity in females housed in both long and short photoperiod. Exposure to SP resulted in high levels of aggression regardless of the endocrine state of the animal or the measure used to quantify aggression. In contrast, administration of estradiol to hamsters housed in LP significantly reduced aggression. The data of the present study support the hypothesis that SP-housed females are more aggressive than LP-housed females because SP exposure renders females insensitive to the aggression-reducing effects of ovarian hormones.     

Pineal-dependent and -independent effects of photoperiod on immune function in Siberian hamsters (Phodopus sungorus)

Siberian hamsters (Phodopus sungorus) exhibit reproductive and immunological responses to photoperiod. Short (<10-h light/day) days induce gonadal atrophy, increase leukocyte concentrations, and attenuate thermoregulatory and behavioral responses to infection. Whereas hamster reproductive responses to photoperiod are dependent on pineal melatonin secretion, the role of the pineal in short-day induced changes in immune function is not fully understood. To examine this, adult hamsters were pinealectomized (PINx) or sham-PINx, and transferred to short days (9-h light/day; SD) or kept in their natal long-day (15-h light/day; LD) photoperiod. Intact and PINx hamsters housed in LD maintained large testes over the next 12 weeks; sham-PINx hamsters exhibited gonadal regression in SD, and PINx abolished this effect. Among pineal-intact hamsters, blood samples revealed increases in leukocyte, lymphocyte, CD62L+ lymphocyte, and T cell counts in SD relative to LD; PINx did not affect leukocyte numbers in LD hamsters, but abolished the SD increase in these measures. Hamsters were then treated with bacterial lipopolysaccharide (LPS), which induced thermoregulatory (fever), behavioral (anorexia, reductions in nest building), and somatic (weight loss) sickness responses in all groups. Among pineal-intact hamsters, febrile and behavioral responses to LPS were attenuated in SD relative to LD. PINx did not affect sickness responses to LPS in LD hamsters, but abolished the ameliorating effects of SD on behavioral responses to LPS. Surprisingly, PINx failed to abolish the effect of SD on fever. In common with the reproductive system, PINx induces the LD phenotype in most aspects of the immune system. The pineal gland is required for photoperiodic regulation of circulating leukocytes and neural-immune interactions that mediate select aspects of sickness behaviors.     

Cold prevents the light induced inactivation of pineal N-acetyltransferase in the Djungarian hamster,Phodopus sungorus

Summary In the Djungarian hamster seasonal acclimatization is primarily controlled by photoperiod, but exposure to low ambient temperature amplifies the intensity and duration of short day-induced winter adaptations. The aim of this study was to test, whether the pineal gland is involved in integrating both environmental cues. Exposure of hamsters to cold (0 °C) reduces the sensitivity of the pineal gland to light at night and prevents inactivation of N-acetyltransferase (NAT). The parallel time course of NAT activity and plasma norepinephrine content suggests that circulating catecholamines may stimulate melatonin synthesis under cold load.Abbreviations NAT N-acetyltransferase - NE norepinephrine - T _a ambient temperature     

Differential alteration of the reproductive axis by testosterone and estrogen in peripubertal and adult male Siberian hamsters (Phodopus sungorus)

In male Siberian hamsters, administration of adult physiological levels of testosterone (T) and estrogen (E2) to juveniles inhibited pubertal onset by distinct pathways. It is presently unclear if T and E2 also exert an inhibitory effect on the reproductive function of sexually mature and sexually maturing hamsters. This study aims to determine if there is an age-dependent decline in the sensitivity of the hypothalamic-pituitary-gonadal (HPG) axis to these inhibitory steroids and if their actions remain distinct. Peripubertal and adult male Siberian hamsters were implanted with a silastic capsule containing T, E2, or cholesterol (Ch, control). Testosterone treatment significantly reduced testes mass and length and impaired spermatogenesis in both ages. In contrast, E2 treatment reduced testes mass only in peripubertal, but not adult, animals. In fact, E2 treatment significantly increased testes mass in adults without altering spermatogenesis. In addition, circulating E2 is very high immediately prior to pubertal onset and declines thereafter. Our results showed the inhibitory effects of T persist into adulthood whereas those of E2 subside as the animals become sexually mature. The decreased sensitivity of the HPG axis to the inhibitory effects of E2 in adult animals and the high level of circulating E2 immediately prior to pubertal onset suggest E2 may play an important role in the regulation of puberty in this species.     

Housing condition alters immunological and reproductive responses to day length in Siberian hamsters (Phodopus sungorus)

During winter, increased thermoregulatory demands coincide with limited food availability necessitating physiological tradeoffs among expensive physiological processes resulting in seasonal breeding among small mammals. In the laboratory, short winter-like day lengths induce regression of the reproductive tract, but also enhance many aspects of immune function. It remains unspecified the extent to which bolstered immune responses in short days represent enhanced immune function per se compared to long days or represents energetic disinhibition mediated by the regression of the reproductive tract. Cohabitation of male Siberian hamsters with intact female conspecifics can block short-day reproductive regression. We sought to determine whether female cohabitation could also block the enhanced immune function associated with short days. Adult male Siberian hamsters were housed in long or short day lengths in one of three housing conditions: (1) single-housed, (2) housed with a same sex littermate, or (3) housed with an ovariectomized female. Delayed-type hypersensitivity (DTH) responses were assessed after 8 weeks of photoperiod treatment. Housing with an ovariectomized female was not sufficient to block short-day reproductive regression, but prevented short-day enhancement of DTH responses. Housing with a male littermate did not alter reproductive or immune responses in either photoperiod. These data suggest that short day enhancement of immune function is independent of photoperiod-mediated changes in the reproductive system.     

Early embryo development in the Siberian hamster (Phodopus sungorus)

Development of preimplantation embryos of the Siberian hamster (Phodopus sungorus) in vivo and in vitro was examined. The timing of early development in vivo was found to be slower than that reported for the golden hamster. Progression through the cleavage stages, cavitation, and hatching from the zona pellucida occurred later, with blastocyst formation beginning on the afternoon of day 4 and uterine attachment occurring early on day 5. In vitro, morulae, and early blastocysts collected on day 4 and cultured in serum-containing medium formed expanded blastocysts and some began to hatch from the zona pellucida. With extended culture, blastocysts attached and formed trophoblast outgrowths. Outgrowth was characterized by an initial migration of small cells from the blastocyst, followed by formation of a sheet of trophoblast giant cells. Differences in the morphology of outgrowth between the hamster and mouse suggest that further comparative studies with the Siberian hamster may be useful.     

Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters

Many psychological disorders comprise a seasonal component. For instance, seasonal affective disorder (SAD) is characterized by depression during autumn and winter. Because hippocampal atrophy may underlie the symptoms of depression and depressive-like behaviors, one goal of this study was to determine whether short days also induce structural changes in the hippocampus using photoperiod responsive rodents — Siberian hamsters. Exposure to short days increases depressive-like responses (increased immobility in the forced swim test) in hamsters. Male hamsters were housed in either short (LD 8:16) or long days (LD 16:8) for 10 weeks and tested in the forced swim test. Brains were removed and processed for Golgi impregnation. HPA axis function may account for photoperiod-related changes in depressive-like responses. Thus, stress reactivity was assessed in another cohort of photoperiod-manipulated animals. Short days reduced soma size and dendritic complexity in the CA1 region. Photoperiod did not induce gross changes in stress reactivity, but an acute stressor disrupted the typical nocturnal peak in cortisol concentrations. These data reveal that immobility induced by exposure to short days is correlated with reduced CA1 cell complexity (and perhaps connectivity). This study is the first to investigate hippocampal changes in the context of short-day induced immobility and may be relevant for understanding psychological disorders with a seasonal component.