Photoperiod and temperature interact to affect the GnRH neuronal system of male prairie voles (Microtus ochrogaster)

Individuals of numerous species limit energy expenditure during winter by inhibiting reproduction and other nonessential functions. To time these adaptations appropriately with the annual cycle, animals rely on environmental cues that predict, well in advance, the onset of winter. The most commonly studied environmental factor that animals use to time reproduction is photoperiod. Rodents housed in short photoperiods in the laboratory or in naturally declining day lengths exhibit pronounced alterations in reproductive function concomitant with alterations in the hypothalamic gonadotropin-releasing hormone neuronal system. Because animals in their natural environment use factors in addition to photoperiod to time reproduction, the present study sought to determine the independent effects of photoperiod and temperature, as well as the interaction between these factors, on reproductive parameters and the GnRH neuronal system. Male prairie voles were housed in either long (LD 16:8) or short (LD 8:16) day lengths for 10 weeks. Animals in each photoperiod were further subdivided into groups housed in either mild (i.e., 20 degrees C) or low (i.e., 8 degrees C) temperatures. As shown with immunohistochemistry, voles that underwent gonadal regression in response to short photoperiods and long-day voles housed in low temperatures (and maintained large gonads) exhibit higher GnRH-immunoreactive (GnRH-ir) neuron numbers in the preoptic area/anterior hypothalamus (POA/AH) relative to all other groups. In addition, voles that underwent gonadal regression in response to both short days and low temperatures did not exhibit an increase in GnRH-ir neuron numbers compared to long-day, mild-temperature controls. These data suggest that photoperiod and temperature interact to influence reproductive function potentially by alterations of the GnRH neuronal system.     

Photoperiodic regulation of reproductive development in male prairie voles: influence of laboratory breeding

Two populations of male prairie voles, one derived from an outbred laboratory colony and the second consisting of F1 offspring of wild-trapped voles, were tested for responsiveness to photoperiod. Animals were reared from birth until 35 days of age either in 16L:8D or 8L:16D photoperiods. Short day lengths did not affect the reproductive apparatus of the laboratory-strain voles; however, offspring of wild-caught voles manifested arrested development of the reproductive system in short photoperiods. These results suggest that selection processes associated with laboratory husbandry can alter responsiveness to photoperiod; the use of wild-trapped animals or their F1 progeny is indicated in photoperiodism research.     

Hormonal regulation of the annual pelage color cycle in the Djungarian hamster, Phodopus sungorus. I. Role of the gonads and pituitary

The Djungarian hamster exhibits an agouti pelage in the summer and a predominantly white pelage in the winter. This pelage color cycle is known to be regulated by the length of the daily photoperiod probably acting through the pineal gland, as is the seasonal cycle of reproductive function with which it is closely correlated ( Figala et al., '73; Hoffmann, ' 78b ). The possibility of a causal relationship between the decline in gonadal hormone secretion and the coat color change occurring in short photoperiod was examined. Gonadectomized and intact male and female hamsters were exposed to either long (16L:8D) or short ( 10L : 14D ) photoperiod for several months. Gonadectomy neither induced the change to the winter pelage color in long photoperiod-housed animals, nor prevented either the change to the winter pelage or the spontaneous return to summer pelage color in short photoperiod-housed animals. Chronic implants of testosterone in castrated males delayed and attenuated the short photoperiod-induced coat color change. Administration of ovine prolactin (100 micrograms/day) stimulated pigmentation in hamsters with the winter pelage, whereas administration of a alpha MSH (30 micrograms/day) was without effect. These results suggest that changes in pelage color may be regulated largely by changes in pituitary prolactin secretion and modified to some extent by changes in gonadal steroid hormone secretion.     

Photoperiod and temperature can regulate body mass, serum leptin concentration, and uncoupling protein 1 in Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus)

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in wild small mammals. In this study, we performed a factorial experiment (temperature x photoperiod) in which Brandt's voles and Mongolian gerbils were acclimated to different photoperiods (long photoperiod, 16L : 8D; short photoperiod, 8L : 16D) and temperatures (warm, 23 degrees C; cold, 5 degrees C) to test the hypothesis that photoperiod, temperature, or both together can trigger seasonal changes in serum leptin level, body mass, thermogenesis, and energy intake. Our data demonstrate that Brandt's voles showed a remarkable decrease in body mass in both the cold and a short photoperiod. However, no significant changes in body mass were found for gerbils exposed to similar conditions. The short photoperiod induced a decrease in serum leptin levels for both voles and gerbils that might contribute to an increase in energy intake. Furthermore, the short photoperiod induced an increase of uncoupling protein 1 (UCP1) content for both voles and gerbils, and cold can further enhance the increase in voles. No interactions between photoperiod and temperature were detected for the two species. Brandt's voles can decrease their body mass through changes in energy intake and expenditure, while Mongolian gerbils can keep body mass relatively stable by balancing energy metabolism under winterlike conditions. Leptin was potentially involved in the regulation of body mass and thermogenic capacity for the two species.     

Photoperiod influences reproduction in the prairie vole (Microtus ochrogaster)

Four experiments examined the role of photoperiod in the regulation of seasonal breeding in the prairie vole. Adult male voles maintained in short (8L:16D) as compared to long (16L:8D) photoperiods for 10 wk had reduced testicular and seminal vesicle weights, but fertility was not impaired. Male prairie voles reared from birth until 35 days of age in short as compared to long photoperiods also had reduced testicular and seminal vesicle weights, as well as diminished fertility. The incidence of pregnancy did not differ between long- and short-day female voles paired for 6 days with long- or short-day males (93%, 86%, 89%, and 88%, respectively). Photoperiod did not affect the incidence or the timing of postpartum pregnancies in long- or short-day females paired with long-day males through the birth of several litters. Adult male prairie voles retain only marginal sensitivity to short photoperiods, maturing males are highly responsive to short days, and adult females are insensitive to photoperiod. These data suggest that termination of the breeding season in the autumn may be due to the lack of fecund males in the population.     

Photoperiodic regulation in energy intake, thermogenesis and body mass in root voles (Microtus oeconomus)

The present study was designed to examine whether photoperiod alone was effective to induce seasonal regulations in physiology in root voles (Microtus oeconomus) from the Qinghai-Tibetan plateau noted for its extreme cold environment. Root voles were randomly assigned into either long photoperiod (LD; 16L:8D) or short photoperiod (SD; 8L:16D) for 4 weeks at constant temperature (20 degrees C). At the end of acclimation, SD voles showed lower body mass and body fat coupled with higher energy intake than LD voles. SD greatly enhanced thermogenic capacities in root voles, as indicated by elevated basal metabolic rate (BMR), nonshivering thermogenesis (NST), mitochondrial protein content and uncoupling protein-1 (UCP1) content in brown adipose tissue (BAT). Although no variations in serum leptin levels were found between SD and LD voles, serum leptin levels were positively correlated with body mass and body fat mass, and negatively correlated with energy intake and UCP1 content in BAT, respectively. To summarize, SD alone is effective in inducing higher thermogenic capacities and energy intake coupled with lower body mass and body fat mass in root voles. Leptin is potentially involved in the photoperiod induced body mass regulation and thermogenesis in root voles.     

Effects of duration of daily illumination on reproductive organs and fertility of the meadow vole (Microtus pennsylvanicus).

The objective of this study was to determine the optimum simple, constant photoperiod for voles in a laboratory colony. Voles from an established colony maintained at 22 degrees C with a photoperiod of 14:10 hours of light:dark were transferred at 50 days of age to a photoperiod of 12:12, 14:10, 16:8 or 18:6 hours of light:dark. From Day 96 to Day 102, the 9--10 females per treatment group were paired with a male. Body and gonadal weights, spermatogenesis, ovarian activity and pregnancy were evaluated on Day 110. Reproductive function and body weight of both male and female voles maintained on a photoperiod of 16:8 exceeded (p less than 0.05) values for voles exposed to 12:12 hours of light:dark and tended to be more favorable than for voles in the 14:10 and 18:6 groups.     

Role of short photoperiod and cold exposure in regulating daily torpor in Djungarian hamsters

1. Male and female Djungarian hamsters (Phodopus sungorus) were gonadectomized or sham-operated after 12 weeks of exposure to short photoperiods (10L:14D). Half of the animals were single housed and transferred to a cold environment (7 degrees C) at week 13 of short days and half were transferred to cold at week 21. The time courses of short photoperiod induced seasonal changes in body weight, pelage color stage, and daily torpor were monitored periodically until the experiment was terminated after 34 weeks of short days. 2. The total duration of short photoperiod exposure was of primary importance compared to the duration of cold exposure in regulating seasonal changes in the frequency of daily torpor, body weight and pelage color exhibited by male and female Djungarian hamsters; that is, the change from long to short days was much more effective as a seasonal time cue than was the onset of cold exposure. 3. Gonadectomy did not prevent the occurrence of seasonal torpor in hamsters of either sex, indicating that these cycles are regulated by a time measuring mechanism (seasonal clock) that is largely independent of the gonadal cycle. However, castration did influence certain aspects of the body weight and torpor cycles exhibited by male hamsters. 4. Some castrated animals showed a delay in terminating the torpor season lending further support to the hypothesis that the spontaneous recrudescence of the testes which occurs toward the end of the torpor season may play a role in the termination of torpor in males.(ABSTRACT TRUNCATED AT 250 WORDS)     

Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice

In three genuses and four species of rodents, housing in winter-like short days (8L:16D) increases male aggressive behavior. In all of these species, males undergo short-day induced regression of the reproductive system. Some studies, however, suggest that the effect of photoperiod on aggression may be independent of reproductive responses. We examined the effects of photoperiod on aggressive behavior in California mice (Peromyscus californicus), which do not display reproductive responsiveness to short days. As expected, short days had no effect on plasma testosterone. Estrogen receptor alpha and estrogen receptor beta immunostaining did not differ in the lateral septum, medial preoptic area, bed nucleus of the stria terminalis, or medial amygdala. However, males housed in short days were significantly more aggressive than males housed in long days. Similar to previous work in beach mice (Peromyscus polionotus), estradiol rapidly increased aggression when male California mice were housed in short days but not when housed in long days. These data suggest that the effects of photoperiod on aggression and estrogen signaling are independent of reproductive responses. The rapid action of estradiol on aggression in short-day mice also suggests that nongenomic mechanisms mediate the effects of estrogens in short days.     

The thalamic intergeniculate leaflet mediates locomotor activity-induced reversal of phenotype in photoperiod nonresponsive Siberian hamsters

The role of the intergeniculate leaflet of the thalamus (IGL) in photoperiod responsiveness was examined in a laboratory-selected line of photoperiod nonresponsive (NR) Siberian hamsters. NR hamsters fail to exhibit typical winter-type responses (i.e., gonadal regression and development of winter-type pelage) when exposed to short day lengths (e.g., 10 h of light/day). Earlier studies revealed that NR hamsters will exhibit winter-type responses when exposed to short photoperiod if they are given free access to a running wheel. The present study tested the hypothesis that this locomotor activity-induced reversal of phenotype is dependent on the IGL. Male NR hamsters underwent destruction of the IGL prior to being housed in short day lengths in cages equipped with running wheels. Activity rhythms were monitored for 8 weeks, after which time pelage response and paired testes weights were obtained. In contrast to sham-operated NR animals given access to running wheels, IGL-ablated animals showed no increase in the duration of nocturnal running wheel activity and became active later in the night than sham-lesioned animals. Lesioned animals also failed to exhibit the typical short photoperiod-induced gonadal regression and pelage molt. The results implicate the IGL in the mechanism by which running wheel activity can influence photoperiodic responses.     

The effects of running activity on the reproductive axes of rodents

Access to a running wheel causes gonadal recrudescence in Syrian hamsters whose reproductive axes have been suppressed by housing them under short day lengths (Borer et al. 1983). The first experiment tested the generality of this phenomenon in a population of rodents that is genetically heterogeneous for reproductive photoresponsiveness. Male meadow voles (Microtus pennsylvanicus) of the two extreme phenotypes — reproductively photoresponsive and non-responsive — were either provided with a running wheel or housed without one. After 4 weeks with a wheel, the responsive voles had recovered full reproductive function, while the reproductive axes of responsive voles housed without wheels remained suppressed. Three experiments queried whether the use of a wheel would have reproductively stimulative effects in other rodents. First, intact male mice given access to wheels showed no increase in testis size when compared to mice housed without wheels. Likewise, locomotor activity had no effect on male rats whose testes were partially regressed in response to testosterone implants or on female mice whose estrous cycles were pheromonally suppressed by housing them in groups. Thus the neuroendocrine pathway used by locomotor activity to enhance the secretion of gonadotropin is specifically allied with the pathway used by photoperiod to control GnRH secretion.Abbreviations GnRH gonadotropin-releasing hormone - LH luteinizing hormone     

Phenotypic differences in the GnRH neuronal system of deer mice Peromyscus maniculatus under a natural short photoperiod

The neural mechanisms by which short photoperiod induces gonadal regression among seasonally breeding mammals are not well understood. One hypothesis suggests that the proximate cause of seasonal gonadal regression is a photoperiod-induced modification in GnRH secretion. This hypothesis is indirectly supported by our recent findings using immunocytochemistry which identified specific photoperiod-induced adjustments in the number and morphology of GnRH containing neurones between reproductively competent and reproductively regressed laboratory housed male deer mice. Herein, we report that the GnRH neuronal system is similarly affected in reproductively responsive and nonresponsive wild male deer mice Peromyscus maniculatus exposed to a natural short photoperiod. The distribution of immunoreactive (IR)-GnRH neurones was nearly identical in field caught animals and those housed under artificial photoperiod in the laboratory. Compared with reproductively nonresponsive males, reproductively responsive mice from the field population possessed a greater total number of IR-GnRH neurones, a greater number of IR-GnRH neurones within the lateral hypothalamus, and a greater proportion of bipolar IR-GnRH neurones. Each of these distributional and morphological characters was consistent with our findings in laboratory housed male deer mice exposed to an artificial short photoperiod. Taken together, these data underscore the validity of using an artificial photoperiod to evaluate seasonal adjustments in reproductive function in the laboratory.     

Low ambient temperature accelerates short-day responses in Siberian hamsters by altering responsiveness to melatonin

Exposure to low ambient temperatures (Ta) accelerates appearance of the winter phenotype in Siberian hamsters transferred from long to short day lengths. Because melatonin transduces the effects of day length on the neuroendocrine axis, the authors assessed whether low Ta promotes the transition to winterlike traits by accelerating the onset of increased nocturnal melatonin secretion or by enhancing responsiveness to melatonin in short day lengths. Male hamsters were transferred from 16L (16 h light/day) to 8L (8 h light/day) photoperiods and held at 5 degrees C or 22 degrees C. Locomotor activity was recorded continuously, and body mass, testis size, and pelage color were determined biweekly for 8 weeks. The duration of nocturnal locomotion (alpha), a reliable indicator of the duration of nocturnal melatonin secretion, lengthened significantly earlier in hamsters exposed to a Ta of 5 degrees C than 22 degrees C. Cold exposure increased the proportion of hamsters that were photoresponsive: gonadal regression in short days increased from 44% at 22 degrees C to 81% at 5 degrees C (p < 0.05); low Ta did not, however, accelerate testicular regression in animals that were photoresponsive. Nonphotoresponsive animals at 5 degrees C temporarily had longer alphas during the first 4 weeks in short days and significant decreases in body mass and testicular size that were reversed during the ensuing weeks when alpha decreased. In a 2nd experiment, pinealectomized male hamsters infused for 10 h/day with melatonin for 2 weeks had significantly lower body and testes masses when maintained at 5 degrees C but not 22 degrees C. Low-ambient temperature appears to accelerate the appearance of the winter phenotype primarily by increasing target tissue responsiveness to melatonin and to a lesser extent by augmenting the rate at which the duration of nocturnal melatonin secretion increases in short day lengths.     

Role of photoperiod in reproductive maturation and peripubertal hormone concentrations in male collared lemmings (Dicrostonyx groenlandicus).

Onset of sexual maturation was determined in weanling male collared lemmings exposed to one of three experimental regimens of different photoperiods before and after weaning. Animals gestated in photoperiods of either 16 h light:8 h dark or 8 h light:16 h dark. Those from 16 h light:8 h dark were transferred at 19 days of age to either 20 h light:4 h dark or 8 h light:16 h dark; those gestated under 8 h light: 16 h dark remained in that photoperiod throughout the experiment. After exposure for 15, 20, 25 or 30 days to the postweaning photoperiod, animals were killed and the following parameters assessed: body weight, testes weight, seminal vesicle weight, the presence or absence of epididymal spermatozoa and serum concentrations of prolactin, testosterone and corticosterone. All parameters except serum testosterone were significantly influenced by photoperiod. Animals housed under 8 h light:16 h dark had significantly greater body weights than those housed under 20 h light:4 h dark, a response that differs from that reported for other arvicoline rodents. The group gestated on 16 h light:8 h dark and transferred on day 19 to 8 h light:16 h dark had lower testes and seminal vesicle weights than the other two groups, and mature spermatozoa in the epididymides appeared 5 days later than in the 20 h light:4 h dark group. Serum prolactin was largely undetectable in animals from both 8 h light:16 h dark groups, but all males housed in 20 h light:4 h dark had 2.0-15.0 ng prolactin ml-1. Concentration of serum corticosterone was higher in animals weaned into long photoperiod, and decreased with age. These data indicate that weanling male D. groenlandicus are reproductively photoresponsive, but use a decrease in photoperiod, not static short-photoperiod exposure, to alter the rate of development. Prolactin was largely undetectable in animals exposed to short photoperiod, indicating that high concentrations of this hormone are not important for maturation. Low prolactin concentrations in animals in short photoperiods may mediate the annual moult to white pelage. The short-photoperiod-mediated decrease in corticosterone may play a role in seasonal changes in body weight and composition.     

Cross-fostering of voles demonstrates in utero effect of photoperiod

Postweaning body growth and reproductive tract weight of montane voles raised from birth in 14 h light/day are modulated by the photoperiod to which the voles' mothers were exposed while pregnant. This effect could result from factors acting in utero or during lactation, as a result of a change in photoperiod experienced by the mother on the day she gave birth. To distinguish between these hypotheses, male voles exposed to short or long photoperiods during gestation were raised by foster mothers that had been exposed to different photoperiods while pregnant. The differences in body weight, total length, and reproductive tract weight between voles at 74 days of age can be attributed to factors acting in utero. The effects of the gestational photoperiod are not manifested in the patterns of growth until after weaning.     

光周期对布氏田鼠幼仔生长发育的影响

通过比较法对实验室内布氏田鼠 (Microtusbrandti)幼仔生长发育与光周期关系的研究表明 ,尽管出生和断乳时的窝仔数及断乳时窝仔存活率不受光周期的影响 (t test,P >0 0 5 ) ,每种光周期条件下出生和断乳时雌雄比例差异不显著 (Chi square检验 ,P >0 0 5 ) ,不同光周期间雄性比例无明显差异 (百分数的检验 ,P >0 0 5 ) ,但是 ,随着幼仔的生长 ,出生并饲养在长光照周期 (LD ,14L∶10D)下的个体体重、体长和肥满度显著大于短光照周期 (SD ,10L∶14D)下的幼体 ,尤在出生 9或 14天以后的各阶段 (t test,P <0 0 5 )。在 6 0日龄时 ,LD雄鼠的睾丸、附睾及储精囊成熟指数显著高于SD鼠 (t test,睾丸 ,t =3 30 9,df =14,P <0 0 1;附睾 ,t=3 6 2 2 ,df =14,P <0 0 1;储精囊 ,t=3 379,df =14,P <0 0 1)。但LD组的皮毛厚度和绒毛长度显著低于SD组 (t test,皮毛厚度t=- 5 185 ,df =14,P <0 0 1;绒毛长度t=- 2 415 ,df =14,P <0 0 5 )。作者认为体重、肥满度和性腺成熟指数 (GSI)高的LD鼠较SD鼠更适应于繁殖期的繁殖生存 ;而生长发育缓慢 ,皮毛厚度、绒毛长度高的SD鼠更能适应越冬生存。在自然环境中 ,光周期可能被布氏田鼠作为季节环境变化的信号 ,使其在形态和生殖方面提前作好准备 ,采取不同的策略以适     

Influence of photoperiod, nutrition and water availability on reproduction of male California voles (Microtus californicus)

Male California voles were maintained in long (14L:10D) or short photoperiods (10L:14D) for 10 weeks and fed a standard diet of rabbit chow and water ad libitum. One additional group in each photoperiod received the standard diet plus supplements of spinach 3 times weekly. A fifth group was housed in 14L:10D and fed the standard diet, but for 10 weeks water availability was restricted to several hours each morning. Testes and seminal vesicles were heaviest in long-day voles fed spinach supplements and lightest in short-day voles fed only the standard diet; the latter animals manifested reduced testicular spermatogenesis. Testicular weights were also depressed in voles with restricted access to water. It is suggested that photoperiods that simulate those of winter induce regression of the reproductive organs of male California voles but the availability of green vegetation counteracts the inhibitory effects of short daylengths.     

Pineal and photoperiodic influences on fat deposition, pelage, and testicular activity in male meadow voles

Pinealectomy completely prevented gonadal regression as well as reduction in body weight and white adipose tissue content of the gonadal and retroperitoneal fat deposits in male meadow voles transferred from long to short day lengths. Pineal influences on pelage characteristics depended on which parameter was assessed. For instance, the increase in guard hair length observed in short-day control voles was blocked by pinealectomy; however, a similar increase in underhair length was unaffected by removal of the pineal gland. Photoperiod-dependent changes in fat deposition, testicular activity, and guard hair length presumably rely on altered pineal secretory activity to transduce the effects of day length on the neuroendocrine axis; however, mechanisms independent of pineal activity may be capable of mediating photoperiodic control of underhair growth.     

光照和温度对根田鼠褐色脂肪组织产热能力的影响

测定了根田鼠在室内驯化2周后褐色脂肪组织（BAT）的蛋白含量、线粒体蛋白含量和细胞色素C氧化酶活性的变化。动物进行如下4种处理:23℃,16L:8D;23℃,8L：16D;5℃,16L：8D和5℃,8L:16D.。结果表明,短光照可刺激根田鼠的BAT线粒体细胞色素C氧化酶的活性增加;低温驯化可导致根田鼠的BAT线粒体蛋白含量增加;短光照加低温可进一步促进酶的活性增加。结合个体水平的产热特点,说明根田鼠在产热能力的季节驯化过程中,光周期是一主要的季节调节信号,环境温度进一步增强光照的作用,环境温度和光周期共同作用以诱导其产热能力等方面的生理调节。研究结果支持了环境温度和光周期共同作用以调节动物产热变化的学说。     

Effects of photoperiod on energy intake, thermogenesis and body mass in Eothenomys miletus in Hengduan Mountain region

The present study was designed to examine whether photoperiod alone was effective to induce seasonal changes in physiology in voles (Eothenomys.) from the Hengduan Mountain region. Eothenomys miletus were randomly assigned into either long photoperiod (LD; 16L: 8D) or short photoperiod (SD; 8L: 16D) for 4 weeks at constant temperature (25 °C). At the end of acclimation, SD voles showed lower body mass and body fat coupled with higher energy intake than LD voles. SD greatly enhanced the thermogenic capacity of E. miletus, as indicated by an elevated nonshivering thermogenesis (NST), mitochondrial protein in brown adipose tissue (BAT); basal metabolic rate (BMR) was also raised. Although no variations in serum leptin levels were found between SD and LD voles, serum leptin levels were positively correlated with body mass and body fat mass, and negatively correlated with energy intake and UCP1 content in BAT, respectively. To summarize, SD alone is effective in inducing higher thermogenic capacities and energy intake coupled with lower body mass and body fat mass in root voles. Leptin is potentially involved in the photoperiod induced body mass regulation and thermogenesis in E. miletus. Our study shows that SD alone is effective.