Metabolic and genomic adaptations to winter fattening in a primate species, the grey mouse lemur (Microcebus murinus).

AIM: To understand the mechanisms underlying the development of metabolic changes leading to obesity remains a major world health issue. Among such mechanisms, seasonality is quite underestimated although it corresponds to the manifestation of extreme metabolic flexibility in response to a changing environment. Nevertheless, the changes induced by such flexibility are far to be understood, especially at the level of insulin signaling, genomic stability or inflammation. METHODS: Here, we investigated the metabolic regulations displayed by a seasonal primate species, the grey mouse lemur (Microcebus murinus) that exhibits pronounced changes in body mass during the 6-month winter season: a fattening period followed by a spontaneous fat loss, without ever reaching pathological stages. RESULTS: Such body weight modulations result from a combination of behavioral (food intake) and physiological (endocrine changes, switch between carb and lipid oxidation) adjustments that spontaneously operate during winter. Conversely to classical models of obesity, insulin sensitivity is paradoxically preserved during the obesogenic phase. Fat loss is associated with increased metabolic activity, especially in brown adipose tissue, and induced increased oxidative stress associated with telomere length dynamic. Furthermore, liver gene expression analysis revealed regulations in metabolic homeostasis (beta-oxidation, insulin signaling, cholesterol and lipid metabolism) but not for genes involved in inflammatory process (for example, Ifng, Tnf, Nfkb1). CONCLUSION: Altogether, these results show that mouse lemurs undergo deep physiological and genomic seasonal changes, without ever reaching a pathological stage. Further investigation is needed to decipher the underlying mechanisms, which may well be highly relevant for human therapeutic strategies.

Shortened seasonal photoperiodic cycles accelerate aging of the diurnal and circadian locomotor activity rhythms in a primate.

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.

Body mass loss correlates with cognitive performance in primates under acute caloric restriction conditions.

Brain functions are known to consume high levels of energy, thus, the integrity of cognitive performance can be drastically impacted by acute caloric restriction. In this study, we tested the impact of a 40% caloric restriction on the cognitive abilities of the grey mouse lemur (Microcebus murinus). Twenty-three male mouse lemurs were divided into two groups: 13 control animals (CTL) that were fed with 105kJ/day and 10calorie restricted (CR) animals that received 40% less food (63kJ/day) than the CTL animals. The animals were fed according to their group for 19days. Before treatment, we assessed baseline associative learning capacities, resting metabolic rates and locomotor performance of both animal groups. After treatment, we tested the same functions as well as long-term memory. Our results showed that CR animals had lower learning performance following caloric restriction. The effects of caloric restriction on memory recall varied and depended on the metabolism of the individual animal. Body mass loss was linked to memory test performance in the CR group, and lower performance was observed in individuals losing the most weight. While CR was observed to negatively impact learning, locomotor capacities were preserved in CR animals, and there were higher resting metabolic rates in the CR group. Our data reinforce the strong link between energy allocation and brain function, and suggest that in the context of food shortage, learning capacities could be a limiting parameter in the adaptation to a changing environment.

Redistribution of CB1 cannabinoid receptors during evolution of cholinergic basal forebrain territories and their cortical projection areas: a comparison between the gray mouse lemur (Microcebus murinus, primates) and rat.

Endocannabinoid signaling, mediated by presynaptic CB1 cannabinoid receptors on neurons, is fundamental for the maintenance of synaptic plasticity by modulating neurotransmitter release from axon terminals. In the rodent basal forebrain, CB1 cannabinoid receptor-like immunoreactivity is only harbored by a subpopulation of cholinergic projection neurons. However, endocannabinoid control of cholinergic output from the substantia innominata, coincident target innervation of cholinergic and CB1 cannabinoid receptor-containing afferents, and cholinergic regulation of endocannabinoid synthesis in the hippocampus suggest a significant cholinergic-endocannabinergic interplay. Given the functional importance of the cholinergic modulation of endocannabinoid signaling, here we studied CB1 cannabinoid receptor distribution in cholinergic basal forebrain territories and their cortical projection areas in a prosimian primate, the gray mouse lemur. Perisomatic CB1 cannabinoid receptor immunoreactivity was unequivocally present in non-cholinergic neurons of the olfactory tubercule, and in cholecystokinin-containing interneurons in layers 2/3 of the neocortex. Significantly, CB1 cannabinoid receptor-like immunoreactivity was localized to cholinergic perikarya in the magnocellular basal nucleus. However, cortical cholinergic terminals lacked detectable CB1 cannabinoid receptor levels. A dichotomy of CB1 cannabinoid receptor distribution in frontal (suprasylvian) and parietotemporal (subsylvian) cortices was apparent. In the frontal cortex, CB1 cannabinoid receptor-containing axons concentrated in layers 2/3 and layer 6, while layer 4 and layer 5 were essentially devoid of CB1 cannabinoid receptor immunoreactivity. In contrast, CB1 cannabinoid receptors decorated axons in all layers of the parietotemporal cortex with peak densities in layer 2 and layer 4. In the hippocampus, CB1 cannabinoid receptor-containing terminals concentrated around pyramidal cell somata and proximal dendrites in the CA1-CA3 areas, and granule cell dendrites in the molecular layer of the dentate gyrus. CB1 cannabinoid receptors frequently localized to inhibitory GABAergic terminals while leaving glutamatergic boutons unlabeled. Aging did not affect either the density or layer-specific distribution of CB1 cannabinoid receptor-immunoreactive processes. We concluded that organizing principles of CB1 cannabinoid receptor-containing neurons and their terminal fields within the basal forebrain are evolutionarily conserved between rodents and prosimian primates. In contrast, the areal expansion and cytoarchitectonic differentiation of neocortical subfields in primates is associated with differential cortical patterning of CB1 cannabinoid receptor-containing subcortical and intracortical afferents.

Circadian rhythms in firing rate of individual suprachiasmatic nucleus neurons from adult and middle-aged mice.

The suprachiasmatic nucleus contains a biological clock that drives circadian rhythms in vivo and in vitro. It has been suggested that the suprachiasmatic nucleus is a primary target of the aging process, because age-related changes in behavioral rhythms are mirrored in alterations in circadian pacemaker function. Using long-term, single-cell recording, we assessed the effect of age on firing-rate patterns of individual suprachiasmatic nucleus neurons of young adult (2-4 months) and middle-aged (9-11 months) C3H mice. Individual suprachiasmatic nucleus neurons from adult mice maintained in culture for at least one week exhibited robust circadian rhythms in spontaneous activity that were similar in the free-running period (23.7+/-0.3 h mean+/-S.E.M.) to recordings from neurons dispersed from neonatal tissue, and showed evidence of entrainment to prior light cycles by exhibiting peak activity, in vitro, approximately 4.0+/-0.3 h (mean+/-S.E.M.) after the time of expected light onset. Aging led to a decreased amplitude of impulse activity in dispersed suprachiasmatic nucleus neurons and increased variability in the circadian waveform. From these results we suggest that age-related deterioration in circadian clock function occurs at the level of individual cells, which may account for some of the age-related deficits observed in the expression of behavioral rhythmicity.

Artificially accelerated aging by shortened photoperiod alters early gene expression (Fos) in the suprachiasmatic nucleus and sulfatoxymelatonin excretion in a small primate, Microcebus murinus.

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.

Effect of vomeronasal organ removal on male socio-sexual responses to female in a prosimian primate (Microcebus murinus).

In most mammals, olfactory cues play an important role in regulating socio-sexual behaviors, but the relative contributions of the main olfactory system and the vomeronasal system remain unclear. The lesser mouse lemur, a nocturnal prosimian, possesses well-developed chemosensory structures, including a functional vomeronasal organ (VNO). In this primitive primate, social communication and competition between males for priority access to receptive females includes reliance on urinary chemical cues. To assess the role of the VNO in mediating males' behavioural responses to females, sexually-experienced intact males (C, n = 8) or males deprived of their VNO (VNX, n = 8) were put in pairs and their socio-sexual behaviors in response to a preoestrous female were monitored. Independent of social context (with or without female), VNX males exhibited less sniffing behaviors than C males, but their marking behaviors, although reduced, were not significantly different. Removal of the VNO dramatically reduced the frequency of both sexual behaviors (anogenital investigations, mounts) and intermale aggressive behaviors. However, VNO removal did not impair successful mating and had no effect on plasma testosterone levels. Lastly, VNX males always exhibited a significantly lower general activity level than C males. The decrease in sexual behaviors and the lack of aggressive intermale competition in responses to a preoestrous female possibly proceed from functional disturbances of central nervous areas connected to the vomeronasal system rather than from a chemosensory deficit per se.

Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus.

In the male lesser mouse lemur (Microcebus murinus), a polygamous long-day breeder of which the life span may reach 12-14 years, the effects of aging on socio-sexual relationships were studied on 44 captive animals of various ages. In this primate, new dominance relationships must be established at the beginning of each breeding season. During the breeding season induced by exposure to artificial long days, preoestrous females were introduced into cages of paired males to elicit sexual competition. Sexual behaviors, social interactions through chemical signals, and dominance relationships were recorded in paired males either of similar age (young or aged pairs), or of mixed ages. In all pairs, competition for priority access to females always occurred and dominance relationships were established unrelated to body weight. Although aged animals exhibited significantly less number of sexual and aggressive behaviors, they outranked younger males excepted when reaching oldest age. Independent of male's age, the typical pattern of seasonal rhythm of testosterone was observed, but aged males demonstrated a significant reduction in mean hormonal levels (25.5 +/- 2.8 ng/mL, n = 8) compared to young animals (50 +/- 2.7 ng/mL, n = 8). Moreover, their hormonal response to photoperiod was phase-shifted leading to reduced testosterone values when females entered oestrus. Despite the fact that testosterone levels and sexual behaviors decreased with aging in this primate, older males reached a dominant position, increasing thus their reproductive success.

Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana).

Cycle and gestation lengths, menstruation patterns, female genital swelling characteristics, and male-female consortship durations are reported in a semifree-ranging group of Tonkean macaques (Macaca tonkeana) studied over a 12 year period. In addition, profiles of urinary estrone conjugates (E1C) and immunoreactive pregnanediol glucuronide (PdG) throughout four complete menstrual cycles in two females and three full-term pregnancies are presented. Based on intermenstrual intervals, a mean cycle length of 37-41 days (n = 55 cycles in 10 females) was found. Gestation length averaged 173 days (n = 27 pregnancies in eight females). Measurement of PdG immunoreactivity in urine revealed a cyclic pattern with a 5-15-fold increase between follicular and luteal phase concentrations, suggesting that PdG is a reliable indicator of ovarian cyclicity and luteal function. In contrast to PdG, E1C excretion showed no clear pattern throughout the cycle; however, highest values of E1C were usually found shortly before the onset of the luteal phase PdG rise at the presumed time of ovulation. Levels of both hormones were elevated during the first half of gestation and showed a marked increase throughout the second half, with maximum E1C concentrations being up to 100-fold higher than nonpregnant levels. Consortships by the male and occurrence of female genital swelling were long lasting (on average 5-10 days and 13 days, respectively) and were restricted to the follicular phase of the cycle. The day of maximal swelling and day of detumescence as well as the end of male consortship were closely associated with the periovulatory period. Swellings and consortships were longer following lactational ammenorhea than for subsequent cycles. The evolutionary significance of the cyclical changes undergone by females upon their relations with males is discussed. © 1996 Wiley-Liss, Inc.

Calorie restriction and resveratrol supplementation prevent age-related DNA and RNA oxidative damage in a non-human primate.

Oxidative stress is a key factor in the aging process and in the development of age-related diseases. Because nutritional interventions such as caloric restriction (CR) delay the onset of age-related diseases and increase the lifespan of many species, the impact of a moderate CR was tested on male grey mouse lemur (Microcebus murinus), which have a median survival time of 5.7 years in captivity. The effects of CR on these lemurs were compared with a potential mimetic, resveratrol (RSV), a polyphenol naturally found in grapes. We hypothesized that both CR and RSV impact oxidative DNA and RNA damage compared to standard-fed control (CTL) animals. Adult (3-4 years old) male mouse lemurs were assigned to three dietary groups: a CTL group, a CR group receiving 30% fewer calories than the CTL and a RSV group receiving the CTL diet supplemented with RSV (200 mg·day(-1)·kg(-1)). Oxidative stress was estimated after 3, 9, 15 and 21 months of treatment using the measurement of oxidized nucleosides in urine samples by mass spectrometry. The resting metabolic rate, adjusted for changes in body composition, was also measured to assess the potential relationship between oxygen consumption and oxidative damage markers. This study provides evidence for oxidative stress accumulation with age in grey mouse lemur. Dietary interventions resulted in a short-term increase in oxidative stress levels followed by reduced levels with increasing age. Moreover, in this photoperiod-dependent heterotherm primate, seasonal variations in oxidative stress were observed, which was likely due to a season-dependent, cost-benefit trade-off between torpor use and oxidative stress.

Effects of dietary resveratrol on the sleep-wake cycle in the non-human primate gray mouse lemur (Microcebus murinus).

Converging evidence shows that the non-human primate gray mouse lemur (Microcebus murinus) is ideal for the study of the aging process and for testing the effects of new therapies and dietary interventions on age-associated pathologies. One such dietary supplement is resveratrol (RSV), a dietary polyphenolic compound with several positive effects on metabolic functions and longevity. However, little is known about the effect of RSV on the lemur sleep-wake cycle, which reflects mammalian brain function and health. In the present study, the authors investigated this effect by comparing sleep-wake cycles in adult lemurs based on electroencephalographic (EEG) rhythms. The effect of short-term RSV supplementation on the sleep-wake cycle of mouse lemurs was evaluated in entrained conditions (long-day photoperiods, light:dark 14:10). After 3 wks of RSV supplementation, the animals exhibited a significantly increased proportion of active-wake time, occurring mainly during the resting phase of the sleep-wake cycle (+163%). The increase in active-wake time with RSV supplementation was accompanied by a significant reduction of both paradoxical sleep (-95%) and slow-wave sleep (-38%). These changes mainly occurred during the resting phase of the sleep-wake cycle (RSV supplementation induced negligible changes in active-wake time during the active phase of the sleep-wake cycle). The present data suggest that RSV may be a potent regulator of sleep-wake rhythms and could be of major interest in the study of sleep perturbations associated with aging and neuropathology.

The grey mouse lemur: a non-human primate model for ageing studies.

The use of non-human primate models is required to understand the ageing process and evaluate new therapies against age-associated pathologies. The present article summarizes all the contributions of the grey mouse lemur Microcebus murinus, a small nocturnal prosimian primate, to the understanding of the mechanisms of ageing. Results from studies of both healthy and pathological ageing research on the grey mouse lemur demonstrated that this animal is a unique model to study age-dependent changes in endocrine systems, biological rhythms, thermoregulation, sensorial, cerebral and cognitive functions.

Physiological responses to chronic heat exposure in an aging non-human primate species, the gray mouse lemur (Microcebus murinus).

Epidemiological evidence related to increased death from hyperthermia suggests higher frailty in the elderly when exposed to high ambient temperatures. Despite the recent awareness of such public health problems, integrative studies investigating the effects of age on the physiological responses to heat wave thermal conditions remain scarce. Daily rhythmicity of core temperature (T(c)) and locomotor activity (LA), as well as parameters representative of energy balance and IGF-1 levels which are involved in the aging process and stress resistance, were monitored in a non-human primate species, the gray mouse lemur (Microcebus murinus). Adult and aged animals, acclimated to long days (LD) or short days (SD), were monitored during 8-day periods of exposure to 25 ° C and 34 ° C. Adult animals displayed efficient coping with heat exposure, regardless of the photoperiod. Hence, efficient responses resulted in decrease of energy intake, energy expenditure, IGF-1 levels and LA levels, promoting hyperthermia avoidance. Positive energy balance was maintained and water turnover did not change significantly after heat exposure. In contrast, while aged animals acclimated to LD responded similarly to adults, aged mouse lemurs acclimated to SD showed great difficulties coping with heat exposure. Indeed, in this group, normothermia impairment was associated with increased T(c) levels, alterations in daily rhythmicity, negative energy balance and increased IGF-1 levels. Impaired responses to heat exposure were seen in aged mouse lemurs acclimated to SD only. The main effects were observed during diurnal resting periods, suggesting decreased capacities with age to dissipate excess body heat. Taken together, these data highlight daily rhythmicity and IGF-1 pathway as main targets in the impaired response to heat exposure in the elderly.

Gender markedly modulates behavioral thermoregulation in a non-human primate species, the mouse lemur (Microcebus murinus).

Age and gender are known to significantly modulate thermoregulatory capacities in mammals, suggesting strong impacts on behavioral adjustments, which are used to minimize the energy costs of thermoregulation. We tested the effects of sex and age on spontaneous choice of ambient temperature (Ta) in a non-human primate species, the mouse lemur (Microcebus murinus). The animals acclimated to both winter and summer photoperiods, two seasons significantly modifying thermoregulation function, were experimented in a thermal gradient device. During winter, adult males did not show preference for warm Tas whereas old males did. In contrast, female mouse lemurs of both age categories exhibited great preferences for warm Tas. Acclimation to summer revealed that males selected colder Ta for the day than during the night. Such behavior did not exist in females. Old females explored and selected warmer nests than adult ones. This study raised novel issues on the effect of gender on thermoregulatory capacities in the mouse lemur. Females probably use behavioral adjustments to limit energy expenditure and might prefer to preserve energy for maternal investment by anticipation of and during the breeding season. Further experiments focusing on female thermoregulatory capacities are needed to better understand the energy challenge that may occur during winter and summer in female mouse lemurs, and whether this trade-off changes during aging.

Non-shivering thermogenesis activation and maintenance in the aging gray mouse lemur (Microcebus murinus).

The cold-induced enhancement of non-shivering thermogenesis (NST), involving brown-adipose tissue (BAT) metabolism, could participate to impair energy balance in the aged gray mouse lemur (Microcebus murinus). We first investigated the age-related modulations of cold-stimulated BAT cell morphology and contents. Then, NST was pharmacologically stimulated to assess whether aging impaired NST activation in the mouse lemur. In reference conditions, the ability to activate NST was preserved during aging in the mouse lemur as BAT morphology and UCP-1 presence did not differ between adult and aged mouse lemurs. Also, the pharmacological activation of NST revealed similar increased levels of O(2) consumption in adult and aged animals, confirming that no age effect could be evidenced on NST activation at 25 degrees C. However, preliminary histological data revealed a lack of lipid resources in one aged individual during cold exposure. Surprisingly, the pharmacological activation of NST revealed an impaired evacuation of the excess body heat in aged animals, associated with increased energy expenditure. Thus, aging seems to be related to decreased capacities in the maintenance of NST rather than in its activation. Energy mobilization could be impaired in the aging mouse lemur but remains to be demonstrated.

Effects of age on thermoregulatory responses during cold exposure in a nonhuman primate, Microcebus murinus.

Cold resistance appears altered with aging. Among existing hypotheses, the impaired capacity in response to cold could be related to an altered regulation of plasma IGF-1 concentration. The combined effects of age and cold exposure were studied in a short-living primate, the gray mouse lemur (Microcebus murinus), which adjusts its energy balance using a daily torpor phase, to avoid high energy cost of normothermia maintenance. Changes in body mass, core temperature, locomotor activity, and caloric intake were monitored under 9-day exposures to 25 degrees C and 12 degrees C in captive animals in winter conditions. Short-term (after 2 days) and long-term (after 9 days) cold-induced changes in IGF-1 levels were also evaluated. In thermoneutral conditions (25 degrees C), general characteristics of the daily rhythm of core temperature were preserved with age. At 12 degrees C, age-related changes were mainly characterized by a deeper hypothermia and an increased frequency of torpor phases, associated with a loss of body mass. A short-term cold-induced decrease in plasma IGF-1 levels was observed. IGF-1 levels returned to basal values after 9 days of cold exposure. No significant effect of age could be evidenced on IGF-1 response. However, IGF-1 levels of cold-exposed aged animals were negatively correlated with the frequency of daily torpor. Responses exhibited by aged mouse lemurs exposed to cold revealed difficulties in the maintenance of normothermia and energy balance and might involve modulations of IGF-1 levels.

Daily hypothermia and torpor in a tropical primate: synchronization by 24-h light-dark cycle.

To study the temporal organization of daily hypothermia and torpor in a nocturnal Malagasy primate, the gray mouse lemur, body temperature (T(b)) and locomotor activity were recorded using telemetry on 39 males held in 24-h light-dark cycles of different photoperiods. Under free-running condition, the circadian T(b) and locomotor activity rhythms had a period shorter than 24 h. Circadian daily hypothermia started by a rapid drop in T(b) (0.24 degrees C/10 min) at the end of subjective night (13 h 25 +/- 20 min) and was characterized by minimal T(b) values 3 h 20 +/- 5 min later. Spontaneous arousal from daily hypothermia occurred at a fixed time (6 h 05 +/- 15 min, n = 7) after the beginning of subjective day. In animals exposed to 24-h light-dark cycles with night duration varying from 10 to 14 h, locomotor activity was strictly restricted to dark time, but the temporal organization of daily hypothermia was not modified, although changes in amplitude of T(b) rhythm were observed. Daily hypothermia was directly induced by light and lasted 5 h 10 +/- 10 min, with minimal T(b) values 3 h 30 +/- 30 min (n = 28) after lights on, on condition that nighttime did not exceed the duration of subjective night. However, in animals exposed to 24-h light-dark cycles with night duration varying from 10 to 5 h, the limit of induction of daily hypothermia by light was ~9 h after the beginning of night. Finally, under short days (14:10-h light-dark cycle), long bouts (6 h 50 +/- 40 min) of actual torpor (minimum T(b) 27.6 +/- 0.9 degrees C) were observed and would involve mechanisms depending on physiological changes induced by short day exposure.

Thermoregulatory responses to variations of photoperiod and ambient temperature in the male lesser mouse lemur: a primitive or an advanced adaptive character?

The lesser mouse lemur, a small Malagasy primate, is exposed to strong seasonal variations in ambient temperature and food availability in its natural habitat. To face these environmental constraints, this nocturnal primate exhibits biological seasonal rhythms that are photoperiodically driven. To determine the role of daylength on thermoregulatory responses to changes in ambient temperature, evaporative water loss (EWL), body temperature (Tb) and oxygen consumption, measured as resting metabolic rate (RMR), were measured in response to ambient temperatures ranging from 5 degrees C to 35 degrees C, in eight males exposed to either short (10L:14D) or long (14L:10D) daylengths in controlled captive conditions. In both photoperiods, EWL, Tb and RMR were significantly modified by ambient temperatures. Exposure to ambient temperatures below 25 degrees C was associated with a decrease in Tb and an increase in RMR, whereas EWL remained constant. Heat exposure caused an increase in Tb and heat loss through evaporative pathways. Thermoregulatory responses to changes in ambient temperature significantly differed according to daylength. Daily variations in Tb and EWL were characterized by high values during the night. During the diurnal rest, lower values were found and a phase of heterothermia occurred in the early morning followed by a spontaneous rewarming. The amplitude of Tb decrease with or without the occurrence of torpor (Tb < 33 degrees C) was dependent on both ambient temperature and photoperiod. This would support the hypothesis of advanced thermoregulatory processes in mouse lemurs in response to selective environmental pressure, the major external cue being photoperiodic variations.

Influence of daylength on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus.

In its natural habitat, Microcebus murinus, a small malagasy prosimian primate, is exposed to seasonal shortage of water and resources. During the winter dry season, animals enter a pronounced fattening period with concurrent decrease in behavioural/physiological activities, whereas the breeding season is restricted to the rainy summer months. To determine the role of daylength on metabolic rate and water loss in this nocturnal primate, we measured body mass, oxygen consumption at 25 degrees C (RMR), circadian water loss through urine output (UO) and evaporation (EWL) in eight males exposed to either short days (8L:16D SD) or long days (14L:10D LD), under controlled captive conditions. Exposure to SD led to a ponderal increase (maximal body mass: 125 +/- 4 g, N = 8), and to significant changes in RMR and water loss, both reaching lowest values after 3 months under SD (0.84 +/- 0.04 ml O2 h-1 g-1 and 38 +/- 0.3 mg H2O g-1 day-1, respectively). Following exposure to LD, body mass decreased to 77 +/- 3 g (N = 8), whereas both RMR and water loss, mainly through EWL, significantly increased (P < 0.001), the highest value occurring after 2 months (1.51 +/- 0.08 ml O2 h-1 g-1 and 87 +/- 7 mgH2O g-1 day-1, respectively). Moreover, independent of daylength, circadian changes in EWL were characterized by significantly reduced values during the diurnal rest. The results demonstrate that daylength variations affect the physiology of this tropical primate, allowing anticipatory adaptation to seasonal environmental constraints.

Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques.

The role of sexual displays in mating strategies and their reliability in indicating the time of ovulation has given rise to multiple explanations in nonhuman primates. In order to discriminate among hypotheses, socio-sexual behaviors were recorded in a semifree ranging group of Tonkean macaques (Macaca tonkeana), together with sexual skin swelling volumes and measurements of urinary concentrations of estrone conjugates and pregnanediol glucuronide. A clear preovulatory peak of urinary estrogen levels occurred 2 days before a defined rise in pregnanediol glucuronide concentrations, indicating that both hormones pointed out the female's ovulatory period. The concept of estrus rightly could be applied to female Tonkean macaques since fluctuations in estrogen levels correlated with cyclic changes in genital swelling sizes and rates of female behavioral attractivity and proceptivity. Males proved to be capable of recognizing the optimal conception period as judged from the occurrence of maximal rates of following behavior, serial matings, and ejaculations during the peri-ovulatory phase. During this time, males succeeded in maintaining exclusive and enduring associations with females. However, consortships occurred precociously, with males starting to affiliate with females, follow, and mount them 1 week before the presumed time of ovulation. These long-lasting consortships appear to be a consequence of the female extended follicular phase. This presumably sexually selected character allowed females to extend conspicuous sexual displays: genital swelling and utterance of an estrous call, which might attract males' attention and arouse them. With regard to female mating tactics, the combination of reliably indicating the time of ovulation to the male and durable periods of competitor exclusion led to reject explanations assuming manipulation about paternity or long-lasting intermale competition incitement in Tonkean macaques. Competition for mates between females also turned out to be an irrelevant factor as it was very low in the species. We conclude that the main function of sexual displays is to herald the approach of ovulation toward available mates.