Short-day Voles Research Articles

Photoperiod induced obesity in the Brandt's vole (Lasiopodomys brandtii): a model of 'healthy obesity'?

ABSTRACTBrandt's voles have an annual cycle of body weight and adiposity. These changes can be induced in the laboratory by manipulation of photoperiod. In the present study, male captive-bred Brandt's voles aged 35 days were acclimated to a short day (SD) photoperiod (8L:16D) for 70 days. A subgroup of individuals (n=16) were implanted with transmitters to monitor physical activity and body temperature. They were then randomly allocated into long day (LD=16L:8D) (n=19, 8 with transmitters) and SD (n=18, 8 with transmitters) groups for an additional 70 days. We monitored aspects of energy balance, glucose and insulin tolerance (GTT and ITT), body composition and organ fat content after exposure to the different photoperiods. LD voles increased in weight for 35 days and then re-established stability at a higher level. At the end of the experiment LD-exposed voles had greater white adipose tissue mass than SD voles (P=0.003). During weight gain they did not differ in their food intake or digestive efficiency; however, daily energy expenditure was significantly reduced in the LD compared with SD animals (ANCOVA, P<0.05) and there was a trend to reduced resting metabolic rate RMR (P=0.075). Physical activity levels were unchanged. Despite different levels of fat storage, the GTT and ITT responses of SD and LD voles were not significantly different, and these traits were not correlated to body fatness. Hence, the photoperiod-induced obesity was independent on disruptions to glucose homeostasis, indicating a potential adaptive decoupling of these states in evolutionary time. Fat content in both the liver and muscle showed no significant difference between LD and SD animals. How voles overcome the common negative aspects of fat storage might make them a useful model for understanding the phenomenon of ‘healthy obesity’.

Effects of Photoperiod and Reproductive Responsiveness on Pituitary Sensitivity to GnRH in Male Prairie Voles (Microtus ochrogaster)

In order to promote survival and reproductive success, many nontropical rodents inhibit reproduction well in advance of winter in response to decreasing day lengths. Male prairie voles (Microtus ochrogaster), small temperate zone rodents, vary in their reproductive response to photoperiod. Some male voles undergo complete gonadal regression when housed in short days (responders) whereas others fail to inhibit reproduction when exposed to short (i.e., <12 h light/day) day lengths (nonresponders). Previous research has shown that phenotypic variation in reproductive response is reflected at the level of the hypothalamic gonadotropin-releasing hormone (GnRH) neuronal system. The present study sought to determine if photoperiod or reproductive condition alters pituitary responsiveness to a GnRH challenge. Animals were housed in either long (LD 16:8) or short (LD 8:16) photoperiods for 10 weeks. Subsequently, short-day voles were separated into responders and nonresponders based on testicular size. To reduce the influence of endogenous testosterone on luteinizing hormone concentrations, half of the animals in each group were castrated. All animals were injected (i.p.) with either 100 or 50 ng of GnRH and a blood sample was collected after 15 min. Although castration resulted in a significant increase in LH concentrations (P<0.05), neither photoperiod nor reproductive condition affected LH concentrations in response to a GnRH challenge (P>0.05). Taken together, these data support the hypothesis that short photoperiods lead to reproductive inhibition by acting at the level of the hypothalamus rather than the pituitary.

Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie voles.

Nontropical animals commonly use the annual change in photoperiod to phase seasonal adjustments that promote survival and reproduction. To cope with the energetic requirements of winter, many rodents alter body mass in anticipation of winter. Photoperiodic adjustments are often mediated by the pineal hormone melatonin; melatonin can exert a primary effect on body mass or secondarily affect body mass by changing blood gonadal steroid levels. The present study sought to determine if prairie voles (Microtus ochrogaster) alter body mass in response to short photoperiods. The role of the gonads in body mass regulation was also assessed. In experiment 1, males housed in short days increased body mass at a greater rate than long-day animals. Gonadectomy enhanced the body mass gain in short-day voles. These data suggest that the gonads contribute to short photoperiod-induced changes in body mass in male voles. In experiment 2, females housed in short days increased body mass at a greater rate than long-day animals, regardless of whether the animals were ovariectomized. Ovariectomy did not affect body mass in either long- or short-day animals, suggesting that the ovaries do not contribute to photoperiod-mediated changes in body mass in female prairie voles. Taken together, these studies suggest that male and female prairie voles use photoperiodic information to time seasonal changes in body mass.

Photoperiod and population density interact to affect reproductive and immune function in male prairie voles.

Seasonal breeding of rodents is often associated with changes in adrenal function; altered adrenal function could account, in part, for seasonal changes in immune function and, ultimately, influence seasonal fluctuations in survival. Animals commonly monitor the annual change in photoperiod to ascertain the time of year and to make appropriate seasonal adjustments in physiology and behavior. Several extrinsic factors affect reproductive responsiveness to photoperiod. The interaction between population density and reproductive and adrenal responsiveness to photoperiod was assessed in the present experiment. Adult male prairie voles (Microtus ochrogaster) were maintained individually for 10 wk in long [light:dark (LD) 16:8] or short (LD 8:16) photoperiods in rooms with either high (10.96 animals/m3) or low (0.18 animals/m3) population densities. Regardless of population density, short-day voles regressed the size of their reproductive organs; reproductive organ masses were higher in long-day voles housed in high-density compared with low-density rooms. Paired adrenal masses were reduced in short-day voles, but were unaffected by population density; serum corticosterone concentrations were significantly elevated in short-day compared with long-day animals. In both photoperiods, basal blood corticosterone levels were higher in voles from low-density compared with high-density rooms. Splenic masses were unaffected by day length, but were elevated among high-density animals. Similarly, serum immunoglobulin (IgG) levels were elevated among high-density animals. These results suggest that population density per se, in the absence of behavioral interactions, can affect reproductive size, and possibly function, in long-day conditions, and that prairie voles, which are highly social, exhibit higher corticosterone and lower IgG levels in low compared with high densities. These results may be important in understanding arvicoline population fluctuations, as well as improving animal husbandry practices in the lab.

Photoperiodic Effects on Steroid Negative Feedback in Female Prairie Voles (Microtus ochrogaster)

Breeding in prairie voles is mainly restricted to the autumn and winter of most years. The organization of estrus in female prairie voles is unusual because behavioral estrus is induced by chemosensory stimuli from the mine of adult conspecific males. Isolated females exhibit undetectable levels of estradiol and never display estrous behavior, yet exposure to male urine causes a cascade of endocrine changes that evoke estrogen secretion from the ovaries and estrous behavior within 24 hr. In the prairie vole, the extreme dependence of estrus on chemosensory stimuli raises the possibility that their ovaries may be less prominent in the regulation of gonadotropin secretion than in species with more endogenously organized estrous cycles. The present study examined the contribution of the ovaries in luteinizing hormone (LH) regulation in prairie voles. Females were maintained for 9 weeks in either long (LD 16:8) or short (LD 8:16) photoperiodic conditions, a blood sample was obtained and then animals were either ovariectomized or received a sham procedure. Another blood sample was obtained a week later and assayed for serum LH. Blood serum LH levels were significantly reduced in short-day voles, compared to long day animals. After ovariectomy both long-day and short-day voles exhibited equivalent elevations in LH levels. This study provides evidence that photoperiod is measured in female voles and the ovaries appear to produce sufficient steroids to suppress LH release.

Reproductive status influences odor preferences of the meadow vole, Microtus pennsylvanicus, in winter day lengths

Sporadic winter breeding is a common occurrence in populations of arvicoline rodents. To elaborate the olfactory basis of winter breeding, odor preferences of meadow voles that did or did not develop their reproductive systems in short day lengths were compared. Voles that did not respond to short days with reproductive inhibition were reproductively mature and are termed nonresponders, while voles that did respond to short days with reproductive inhibition were reproductively immature and are termed responders. Nonresponder females preferred odors of nonresponder males over those of nonresponder females and nonresponder female over responder female odors. Nonresponder males preferred nonresponder over responder female odors. The mutual attraction between male – female and female – female nonresponders may facilitate winter breeding and female – female dyad formation for communal rearing of young, respectively. Responder females preferred odors of female responders over those of male responders and responder over nonresponder male odors. Olfactory preferences of nonresponder short-day voles were not equivalent to those of reproductively competent long-day animals. Differences in odor communication between responder and nonresponder voles are attributable only in part to differences in gonadal hormone secretion.

Effects of photoperiod and 6-methoxy-2-benzoxazolinone on male-induced estrus in prairie voles

Prairie voles (Microtus ochrogaster) are characterized as facultative breeders with higher rates of reproductive activities observed during spring and summer than autumn and winter. The environmental factors regulating seasonal breeding in this species remain unspecified. Short day lengths inhibit reproductive organ development in male prairie voles in the laboratory, but these males remain fertile and capable of siring offspring; female prairie voles have been reported to be reproductively unresponsive to day length in the laboratory. The organization of estrus in this species is unusual in that females never display the cyclic changes associated with estrus; rather, female prairie voles require chemosensory stimuli associated with fertile males in order to be induced into estrus. The plant compound, 6-methoxy-2-benzoxazolinone (6-MBOA), is present in vegetatively growing grasses and sedges and acts to trigger reproduction in other rodent species exposed to short days. It was suspected that 6-MBOA present in the laboratory diet may have overridden the effects of photoperiod on female prairie voles in previous laboratory studies. In the present study, the effects of 6-MBOA and photoperiod on estrus induction were examined. Beginning at Week 0, female prairie voles were housed in long (LD 16:8) or short (LD 8:16) photoperiods for 9 weeks, then implanted subcutaneously either with an empty Silastic capsule or one packed with 6-MBOA. A special diet, devoid of 6-MBOA, was available ad lib from Week 5 to the end of the study. At the start of Week 11, a single drop of breeder male urine or distilled water was applied to the external nares of each female daily for 6 consecutive days. Neither exposure to male urine nor to 6-MBOA affected reproductive organ masses in short-day females. In long days, uterine and ovarian masses were elevated as compared to short-day voles. Treatment with male urine, but not 6-MBOA, further stimulated uterine development in long-day females. Taken together, these results document that the reproductive systems of female prairie voles respond to day length, but are not particularly responsive to short-term exposure to 6-MBOA.

Daylength influences pelage and plasma prolactin concentrations but not reproduction in the prairie vole, Microtus ochrogaster.

Short daylengths did not affect testes weight or spermatogenic index in male voles or uterine weight in female voles. Short daylengths did stimulate the growth of a winter pelage in both sexes; short-day voles had longer underhairs and guard hairs and a thicker, more dense pelage than did long-day voles. Plasma prolactin concentrations were five times higher in long-day than in short-day females and 25% higher in long-day males than in short-day males. The effect of short daylength on pelage was prevented by pinealectomy. We suggest that the growth of a winter coat is an obligate adaptation for winter survival, stimulated by exposure to short daylengths, but that changes in breeding activity are facultative and dependent to a greater extent on other cues for seasonal synchronization.

Gonadal and photoperiodic control of seasonal body weight changes in male voles.

After 15 wk in a short photoperiod (10 h of light/day), adult male voles weighed 25% less and consumed 33% less food than did voles in a long photoperiod (14 h light/day). Neither body weight nor food intake differed among long- and short-day castrated voles. After 19 wk, castrated long-day voles weighed less than did intact animals. Voles reduced their body weight during the first 15 wk in the short photoperiod and increased their body mass during the succeeding 15 wk. Body mass of short-day voles was positively correlated with combined testes weight. Voles in the short photoperiod collected less nesting material than did their long-day counterparts at week 31. Pelage characteristics at week 32 were not affected by castration or by photoperiod. We conclude that the decreased body mass of male voles during the late summer, fall, and early winter reflects a decrease in circulating levels of testicular hormones; gonadal recrudescence and increased circulating androgen levels are in part responsible for the subsequent seasonal increase in body weight. Part of the increased body mass in late winter in field populations or in laboratory voles after 15 wk in the short photoperiod is independent of the resumption of gonadal activity. Fluctuations in neural and endocrine processes, rather than availability of food, are the principal factors underlying seasonal changes in energy balance.

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.

Photoperiodic regulation of body mass, food intake, and reproduction in meadow voles.

Adult male voles were maintained for 10 wk in long or short photoperiods (14 or 10 h of light/day). A third group of animals housed in the long photoperiod was implanted with capsules containing melatonin. Body weight and food intake were measured weekly; various tissues were weighed and analyzed at the time of autopsy. After 10 wk, voles in the short photoperiod weighed 20% less and consumed 30% less food than those housed in the long photoperiod. Total body water and lean body mass were reduced in the short-day animals, although the size of the brown adipose tissue was not affected. White adipose tissue lipoprotein lipase (LPL) activity was markedly reduced in the short-day voles who also manifested gonadal regression and suppression of spermatogenesis. Melatonin mimicked the effects of short photoperiods on LPL activity and on lean body mass; other parameters for melatonin-treated animals were intermediate between those of untreated long- and short-day voles. We hypothesize that winter weight losses experienced by meadow voles in the field are mediated by decreases in the duration of the daily photophase and that the reduction in body mass permits overwintering voles to reduce their energy requirements and the amount of time devoted to foraging. At least part of the seasonal decline in body mass appears due to a decrease in gonadal hormone secretion.

Short photoperiods reduce winter energy requirements of the meadow vole, Microtus pennsylvanicus

Adult male voles were maintained for 10 weeks in long or short photoperiods (14 or 10 hr light/day) at 23 degrees C and then for 6 days at 10 degrees C. Short photoperiod voles weighed approximately 20% less and consumed 36% and 42% fewer calories than did long-day animals at 23 degrees C and 10 degrees C, respectively. Relative energy intake (kcal/g body mass) was lower for short-than long-day voles at 10 degrees C. Short-day animals gathered more nesting material than their long-day counterparts at both ambient temperatures. Absolute as well as relative wet weights of interscapular brown adipose tissue were reduced in short-day voles and their testes were regressed. Two types of dorsal pelage hairs were longer in short- than in long-day voles; a dense undergrowth of light gray hairs, present in all short-day voles, was completely absent or only sparsely represented in the pelage of long-day animals. Photoperiod is a major proximate factor mediating winter adaptations of meadow voles: By decreasing body mass and reducing food requirements, short photoperiods presumably diminish winter foraging activity and energy devoted to thermoregulation. Increases in nest-building activity, growth of a winter pelage, and testicular regression are other changes induced by short daylengths that facilitate survival of over-wintering voles.