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Circadian rhythms are ubiquitous attributes across living organisms and allow the coordination of internal biological functions with optimal phases of the environment, suggesting a significant adaptive advantage. The endogenous period called tau lies close to 24 h and is thought to be implicated in individuals' fitness: according to the circadian resonance theory, fitness is reduced when tau gets far from 24 h. In this study, we measured the endogenous period of 142 mouse lemurs (Microcebus murinus), and analyzed how it is related to their survival. We found different effects according to sex and season. No impact of tau on mortality was found in females. However, in males, the deviation of tau from 24 h substantially correlates with an increase in mortality, particularly during the inactive season (winter). These results, comparable to other observations in mice or drosophila, show that captive gray mouse lemurs enjoy better fitness when their circadian period closely matches the environmental periodicity. In addition to their deep implications in health and aging research, these results raise further ecological and evolutionary issues regarding the relationships between fitness and circadian clock.

Among anthropogenic pressures, light pollution altering light/dark cycles and changing the nocturnal component of the environment constitutes a threat for biodiversity. Light pollution is widely spread across the world and continuously growing. However, despite the efforts realized to describe and understand the effects of artificial lighting on fauna, few studies have documented its consequences on biological rhythms, behavioral and physiological functions in nocturnal mammals. To determine the impacts of light pollution on nocturnal mammals an experimental study was conducted on a nocturnal primate, the grey mouse lemur Microcebus murinus. Male mouse lemurs (N = 8) were exposed 14 nights to moonlight treatment and then exposed 14 nights to light pollution treatment. For both treatments, chronobiological parameters related to locomotor activity and core temperature were recorded using telemetric transmitters. In addition, at the end of each treatment, the 14(th) night, nocturnal and feeding behaviors were explored using an infrared camera. Finally, throughout the study, body mass and daily caloric food intake were recorded. For the first time in a nocturnal primate, light pollution was demonstrated to modify daily rhythms of locomotor activity and core temperature especially through phase delays and increases in core temperature. Moreover, nocturnal activity and feeding behaviors patterns were modified negatively. This study suggests that light pollution induces daily desynchronization of biological rhythms and could lead to seasonal desynchronization with potential deleterious consequences for animals in terms of adaptation and anticipation of environmental changes.

The mammalian endogenous circadian clock, the suprachiasmatic nuclei, receives environmental inputs, namely the light-dark cycle, through photopigments located in the eye and from melanopsin-expressing retinal ganglion cells. The authors investigated the influence of light wavelength and intensity on the synchronization of the rest-activity rhythm of the gray mouse lemur, a nocturnal Malagasy primate. Animals were tested at different irradiance levels (320, 45, 13, and 6 nmol x m(-2) x s(- 1)) under several light wavelengths (from 400 to 610 nm). Several parameters including circadian period, activity, and body temperature waveforms were used to assess synchronization to a 12:12 light-dark cycle in comparison to control treatments (12:12 white light or continuous darkness). Entrainment of the circadian rest-activity cycle increased with light intensity. It was more efficient for mid wavelengths relative to shorter or longer wavelengths but not coincident with melanopsin maximal sensitivity, suggesting other photoreceptors are likely involved in lemurs' photoentrainment. The authors obtained a novel synchronization pattern characterized by a clear synchronization to lights-on only without phasing to lights-off. Changes in photo-responsiveness at dusk and dawn highlight differential responses of evening and morning oscillators in the circadian clock.

Deficits in autonomic thermoregulatory capacities have been identified in aged humans and animals, but little is known about the effect of aging on behavioral thermoregulation and the potential effect of season. Preferred ambient temperature (T(a)) in a thermal gradient (available T(a)s from 10 to 30 degrees C) was measured in the mouse lemur, a nocturnal Malagasy primate. Male mouse lemurs (40 adults and 40 aged) were studied under short (SP, resting season) and long photoperiod (LP, breeding season). Additionally, daily body temperature rhythm was telemetrically recorded in 30 individuals of both age categories. In adults exposed to SP, a choice for warm climates was observed, with a mean diurnal T(a) of 26 degrees C. Day-night differences in selected T(a) occurred only in animals exposed to SP. In LP, selection of a warm environment did not seem to be a necessary factor for maintenance of normothermia. Aged animals selected warmer T(a)s than adults during the night like during the day, whatever the photoperiod. In relation to changes in body temperature rhythm according to age, aged animals would select warmer environments possibly to compensate autonomic deficiencies. Further studies on age-related changes in hormonal and cellular functions involved in energy balance and thermoregulation will help decipher the causes of insufficient responses to thermal stress observed in the elderly.

The gray mouse lemur (Microcebus murinus), a prosimian primate, exhibits seasonal rhythms strictly controlled by photoperiodic variations. Previous studies indicated that longevity can be altered by long-term acceleration of seasonal rhythms, providing a model for assessing various aspects of aging. To assess the effect of aging and accelerated aging on the circadian system of this primate, we compared the circadian rhythm of the locomotor activity in adult mouse lemurs (2-4.5 years, n = 9), aged mouse lemurs (5-9 years, n = 10), and adult mouse lemurs that had been exposed from birth to a shortened seasonal photoperiodic cycle (2-4.5 years, n = 7). Compared to adult animals, aged mouse lemurs showed a significant increase in intradaily variability and an advanced activity onset. Aging was characterized by a decrease in amplitude, with both a decrease in nocturnal activity and an increase in daytime activity. When maintained in constant dim red light, aged animals exhibited a shortening of the free-running period (22.8 +/- 0.1 h) compared to adult animals (23.5 +/- 0.1 h). A 3- to 5-year exposure to an accelerated seasonal photoperiodic rhythm ("annual" duration of 5 months) in accelerated mouse lemurs produced disturbances of the locomotor activity rhythm that resembled those of aged mouse lemurs, whether animals were studied in entrained or in free-running conditions. The present study demonstrated a weakened and fragmented locomotor activity rhythm during normal aging in this primate. Increasing the number of expressed seasonal cycles accelerated aging of parameters related to circadian rhythmicity in adult animals.

Due to their differential reproductive investment, males and females often exhibit high differences in energy management. The main hypothesis tested in this study is that short photoperiod-induced fattening in the small primate Microcebus murinus is strongly affected by social cues. Short photoperiod-induced changes in body mass, lean mass and thyroid hormone T4 plasma levels measurements were investigated in wild and captive animals. Individual housing showed that both males and females are able to fatten. Fattening was associated with a slight increase of lean mass that reached a plateau after 3 weeks. In contrast, social grouping led to an inhibition of fattening, even when direct interactions were prevented. This social inhibition was mainly observed in males, especially when housed with females, suggesting that their low weight gain in the wild is due to female dominance. Accordingly, wild and captive animals of both sexes exhibited a decrease in T4 plasma levels, revealing a decrease in energy expenditure. Moreover, testis recrudescence observed after 20 weeks of short photoperiod exposure did not lead to any inhibition of fattening, indicating that males take advantage of female hibernation late in the dry season to fatten and use their fat reserves for the mating competition. Therefore, seasonal fattening may be used by females to prepare for hibernation and by males to prepare for the mating competition.

The role of olfaction/olfactory cues on photoperiodic responses was assessed in Malagasy primate, the gray mouse lemur. When exposed to short photoperiod (SP), this primate demonstrates rapid changes in energy balance as adaptive anticipatory response for winter survival. To follow early changes induced by SP exposure, body mass, food intake, resting metabolism (RMR) and free thyroxin levels in plasma (T4) were measured in males abruptly transferred to SP: six intact males (controls), eight males that underwent bilateral olfactory removal (BOX) and eight males exposed to male urinary cues (U-exposed). To assess the effect of SP exposure, two other groups were maintained for 6 weeks under LP: six controls and six BOX males. Whereas all studied parameters remained constant in controls and BOX males maintained under LP, exposure to SP led to different responses according to groups. In controls, SP exposure led to a regular increase in body mass and after 4 weeks under SP, plasma T4 levels, food consumption and RMR significantly decreased. Even if BOX males demonstrated hyperphagic patterns regardless of the photoperiod, an increase in body mass was also induced by SP exposure but without changes in RMR or food intake that were body mass-dependent. In U-exposed males, body mass gain was significantly reduced while food intake and RMR remained high. In both BOX and U-exposed males, SP exposure led to a transient but high increase in T4 levels compared to controls. These results suggest that olfaction/olfactory cues may delay the SP-mediated changes in energy balance.

In mammals, a number of anatomical and functional changes occur in the circadian timing system with aging. In certain species, aging can be modified by various factors which induce a number of pathological changes. In a small primate, the gray mouse lemur (Microcebus murinus), long-term acceleration of seasonal rhythms by exposing the animals to a shortened photoperiodic regime (up to 2.5 times the natural photoperiodic regime) alters longevity, based on survival curves and morphological changes. This provides a model for challenging the idea that modifications of the circadian pacemaker are related to chronological (years) versus biological (photoperiodic cycles) age. To assess the effect of aging and accelerated aging on the circadian pacemaker of this primate, we measured body weight variations, the daily rhythm in urine 6-sulfatoxymelatonin and the light-induced expression of the immediate early gene (Fos) in the suprachiasmatic nucleus of mouse lemurs that had been exposed to different photoperiodic cycles. Urine samples were collected throughout the day and urine 6-sulfatoxymelatonin levels were measured by radioimmunoassay. Light-induced Fos expression in the suprachiasmatic nucleus was studied by exposing the animals to a 15-min monochromatic pulse of light (500 nm) at saturating or sub-saturating levels of irradiance (10(11) or 10(14) photons/cm(2)/s) during the dark phase. The classical pattern of 6-sulfatoxymelatonin excretion was significantly altered in aged mouse lemurs which failed to show a nocturnal peak. Fos expression following exposure to low levels of irradiance was reduced by 88% in the suprachiasmatic nucleus of aged mouse lemurs. Exposure to higher irradiance levels showed similar results, with a reduction of 66% in Fos expression in the aged animals. Animals subjected to artificially accelerated aging demonstrated the same alterations in melatonin production and Fos response to light as animals that had been maintained in a routine photoperiodic cycle. Our data indicate that there are dramatic changes in melatonin production and in the cellular response to photic input in the suprachiasmatic nucleus of aged mouse lemurs, and that these alterations depend on the number of expressed seasonal cycles rather than on a fixed chronological age. These results provide new insights into the mechanisms underlying artificial accelerated aging at the level of the molecular mechanisms of the biological clock.

To cope with the 6-month dry winter occurring in its natural habitat, the gray mouse lemur (Microcebus murinus), a Malagasy prosimian primate, exhibits a pre-wintering fattening phase that has been previously demonstrated to be dependent on the photoperiod. To assess early changes in energy balance following a photoperiodic shift, food intake (FI), resting metabolic rate (RMR), plasma triglycerides, plasma thyroxine and urinary excretion of cortisol were measured in 12 males and 12 females for 8 weeks following a shift from short (SP: 10 h light/day) to long (LP: 14 h light/day) photoperiod or from LP to SP. Shift from LP to SP led to a high, linear body mass (BM) increase in both sexes, concomitant to an increase in plasma triglycerides and a decrease in plasma thyroxine, while no change in RMR occurred. FI significantly increased from 30 to 40 kcal/day as early as the first week following SP exposure but spontaneously decreased after 4 weeks, reaching minimal values (10 kcal/day) after 14 weeks of SP exposure. Shift from SP to LP led to a decrease in BM and an increase in FI, but both were slow and different between males and females. No change in RMR was observed except a significant increase in males during the first week of LP exposure. However, plasma thyroxine levels and cortisol excretion similarly increased in both sexes following LP exposure. These results suggest that autumnal fattening mainly proceed from changes in FI and in thyroxine secretion triggered by exposure to SP. In contrast, BM loss following LP exposure would be related to seasonal sexual activation rather than to a direct control by photoperiod.

The lesser mouse lemur, a small prosimian primate, exhibits seasonal rhythms strictly controlled by photoperiodic variations. Exposure to day lengths shorter than 12 h results in complete sexual rest, fattening, lethargy, and reduced behavioral activities; whereas exposure to day lengths greater than 12 h induces sexual activity, an increase in behavioral activities, and high hormonal levels. The objective of this study was to test whether long-term acceleration of seasonal rhythms may affect survival and longevity of this primate. In captivity, acceleration of seasonal rhythms was obtained by exposing the animals to an accelerated photoperiodic regimen consisting of 5 months of long photoperiod followed by 3 months of short photoperiod. The age-specific survival rate in animals exposed from birth to accelerated photoperiodic conditions (n = 89) was compared to the age-specific survival rate of animals maintained under a natural photoperiod (n = 68). Independent of sexes, the mean life span (45.5 +/- 2.1 months) and maximal survival (79.3 +/- 3.3 months) were significantly (p < .01) shortened in mouse lemurs exposed to the accelerated photoperiodic cycle compared to those in animals living under annual photoperiod (63.2 +/- 2.5 and 98 +/- 3.9 months for mean life span and maximal survival, respectively). This reduction of about 30% of life span was not accompanied by a desynchronization of biological rhythms under photoperiodic control and was not related to an increase in reproduction or in duration of time spent in active conditions. However, when the number of seasonal cycles experienced by 1 individual is considered rather than chronological age, the mean life span was 5 seasonal cycles and maximum survival reached 9-10 cycles, independent of sex or of photoperiodic regimen. These results suggest that in mouse lemurs, as in other seasonal mammals, longevity may depend on the expression of a fixed number of seasonal cycles rather than on a fixed biological age.

The body weight and sexual activity of the male lesser mouse lemur, a prosimian primate, undergo cyclic changes that are photoperiod-dependent. Exposure to long daylength (LD; 14 h light/day) led to sustained sexual activity, fully developed testes and high plasma testosterone concentrations (228 +/- 25 nmol/l, n = 10). After 14 weeks under LD, a marked decrease in testosterone levels occurred. Gonadal regression was completed within 20 weeks under LD without concomitant changes in body weight. Exposure to short daylength (SD; 8 h light/day) reinforced the sexual quiescence and was associated with a high ponderal gain (from 60 to 110 g). However, independent of the date of gonadal arrest, the sexual activity of males spontaneously resumed at a fixed time after exposure to SD. The testes developed, testosterone concentrations increased to 155 nmol/l and the body weight decreased (from 110 to 80 g) within 20 weeks under SD exposure. The timing for refractoriness appeared very similar under inhibitory and stimulatory photoperiods. This is consistent with the hypothesis that the perception of a critical daylength is used to regulate the timing of the following sexual phase through a mechanism involving photorefractoriness. Contrary to cricetid rodents, a direct response to photoperiodic signals for both body weight and sexual activity were not prevented by olfactory bulb removal in male mouse lemurs. In bulbectomized males (n = 12), sexual activity was stimulated by LD and inhibited by SD. Their plasma testosterone levels, however, significantly differed from those of controls in both photoperiods. Likewise, ponderal cycles remained intact but the fattening phase was delayed and reduced.(ABSTRACT TRUNCATED AT 250 WORDS)

The grey mouse lemur (Microcebus murinus) is a small nocturnal primate exhibiting daily torpor. In constant ambient temperature (22–24 °C), body temperature (Tb) and locomotor activity were monitored by telemetry in animals exposed to short (SP: 10 h light/day) or long (LP: 14 light/day) photoperiods. They were first fed ad libitum for 8 days and then subjected to 80% restricted feeding for 8 more days. During ad libitum feeding, locomotor activity was significantly lower in SP-exposed animals than in LP-exposed animals. Whatever the photoperiod, animals entered daily hypothermia within the first hours following the light onset. Depth of daily hypothermia increased irregularly under SP exposure, whereas minimal daily Tb was constantly above 35 °C under LP exposure. After the transfer from long photoperiod to short photoperiod corresponding to the induction of seasonal fattening, locomotor activity and depth of controlled daily hypothermia did not change significantly. In contrast, food restriction led to a significant increase in locomotor activity and in frequency of daily torpor (Tb<33 °C) and body temperature reached minimum values averaging 25 °C. However, SP-exposed animals exhibited lower minimal daily Tb and higher torpor duration than LP exposed animals. Therefore, daily torpor appears as a rapid response to food restriction occurring whatever the photoperiod, although enhanced by short photoperiod. [Copyright &y& Elsevier]