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Brown fat and nonshivering thermogenesis in the gray mouse lemur (Microcebus murinus).

The gray mouse lemur Microcebus murinus is a rare example of a primate exhibiting daily torpor. In captive animals, we examined the metabolic rate during arousal from torpor and showed that this process involved nonshivering thermogenesis (NST). Under thermoneutrality (28 degrees C), warming-up from daily torpor (body temperature <33 degrees C) involved a rapid (<5 min) increase of O(2) consumption that was proportional to the depth of torpor (n = 8). The injection of a beta-adrenergic agonist (isoproterenol) known to elicit NST induced a dose-dependent increase in metabolic rate (n = 8). Moreover, maximum thermogenesis was increased by cold exposure. For the first time in this species, anatomic and histological examination using an antibody against uncoupling protein (UCP) specifically demonstrated the presence of brown fat. With the use of Western blotting with the same antibody, we showed a likely increase in UCP expression after cold exposure, suggesting that NST is also used to survive low ambient temperatures in this tropical species.

Adipose Tissue, Brown↗

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.

Animals↗

Comparison of the genetic diversity of wild and captive groups of Microcebus murinus using the random amplified polymorphic DNA method.

Continued survival of most animal species depends on population management and active protection. It is generally agreed that, in order to avoid extinction of endangered species, ex situ and in situ conservation must be developed in tandem. However, even though many recommendations have been put forward to promote the survival of captive populations, some rapidly become extinct due to loss of genetic diversity (drift effect). Genetic markers, such as random amplified polymorphic DNA (RAPD) markers, can be applied to rapid testing of many individuals. They also permit analysis of very small amounts of DNA, when small species such as mouse lemurs (Microcebus) are to be tested. Using RAPD markers, we compare genetic diversity in four captive groups of Microcebus murinus to that in a sample of 70 wild mouse lemurs. Following the principles of Mendelian inheritance, each amplified fragment of DNA may be considered as a 'locus' (or an amplifying site). The series of bands amplified by a particular primer in any individual is referred to as the individual's 'profile'. We tested 5 primers, or, in the above terms, we studied 98 different 'loci'. Results showed that the captive groups had lost genetic information with respect to the wild sample. Among the four captive groups, the loss of genetic diversity varied according to their number of founders and/or the management of their captive reproduction. Our study of polymorphism permitted us to establish tools for the genetic management of captive breeding, and for the determination of paternity which frequently give better results than behavioural studies; and simulation of introductions or departures of individuals in one very monomorphic group permitted estimation of future increases in its genetic diversity.

Amino Acid Sequence↗

Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus).

Sexual advertisement calls of male mouse lemurs from two neighbouring demes in a dry deciduous forest of western Madagascar were recorded during the breeding season. Demes were located about 1.5 km apart with no geographic barrier between them. They were characterised morphometrically and genotyped by RAPD fingerprinting. According to univariate and multivariate statistical analysis, demes differed neither in body measurements, nor in the banding patterns produced by RAPD fingerprinting. The acoustic pattern of the advertisement call, however, showed significant differences: Six variables of the frequency and time domain differed between the demes. Discriminant function analysis revealed that one variable, total call duration, was sufficient to classify more than 89% of the calls correctly to the corresponding deme. We postulate that these differences are comparable to dialects in birds, because demes were morphologically and genetically indistinguishable and no barrier prevented genetic exchange between them. Possible explanations for the emergence of dialects in a prosimian species are outlined.

Acoustics↗

Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius).

Parental care should evolve only if fitness benefits exceed fitness costs. In Cheirogaleus medius, a small nocturnal lemur of western Madagascar, we found the peculiar situation of considerable parental care by both sexes, combined with an extremely high rate of extra-pair young (EPY). In this paper, we try to elucidate the costs and benefits of parental care in C. medius, and we discuss hypotheses as to why males might actively participate in raising young, especially with regard to the high rate of EPY. The study was carried out in the dry deciduous forest of western Madagascar between 1996 and 2001. The most important components of parental care in C. medius are babysitting and guarding of the young. Observational data suggest that thermoregulatory demands during the first days after birth and defence from predators may be the driving factors selecting for this infant care behaviour. The reproducing individuals of both sexes incur considerable energetic costs by this behaviour, resulting in reduced fat stores and body condition in comparison to non-reproducing individuals. The reason why males also care for EPY remains elusive. We propose that males might not be able to detect individual relatedness and that they would jeopardise the survival of their own young if they gave no parental care. Alternatively, they might gain advantages other than direct fitness from raising EPY, for example if caring behaviour increases their chances in further reproduction, or if EPY are fathered by close kin.

Animals↗

Mating system in mouse lemurs: theories and facts, using analysis of paternity.

Among nocturnal Malagasy prosimians, the grey mouse lemur (Microcebus murinus) is considered a solitary species which has a promiscuous mating system. Indirect indicators, such as the lack of sexual dimorphism, the overlapping of male and female home ranges with each other, the synchronism of seasonal oestrus and the high relative testes size of males, support the presence of sperm competition. In captivity, an intense sexual precopulatory competition develops among males, leading to the emergence of a dominant male who fathers the majority of the litters. Although multiple mating did occur, the dominant male achieved the majority of the matings on the first day of oestrus. A 'mate-guarding' behaviour, exhibited by the dominant male, was observed in 11 groups out of 15, on only the first day of the vaginal opening and was significantly more often directed towards younger females. Females also played an important role in sexual competition among males, since their presence enhances the aggressive interactions between males. Difference in aggressive behaviours of females, in response to male sexual solicitations, suggests female mate choice. Compared with data from wild animals, it may be hypothesised that alternative mating strategies can be used by male grey mouse lemurs to enhance their reproductive success, depending on the availability and distribution of receptive females.

Animals↗

Cytochrome oxidase 'blobs' and other characteristics of primary visual cortex in a lemuroid primate, Cheirogaleus medius.

We recently obtained the brain of a rare lemuroid primate, Cheirogaleus medius. The brain was not perfused before death, but rather fixed by immersion shortly thereafter. In both flat-mounted and transversely sectioned tissue, we were able to clearly demonstrate periodic zones of high cytochrome oxidase (CO) activity in the primary visual cortex, resembling the so-called 'blobs' described in many other primate species. Our results contrast with a previous report indicating that blobs are absent in Cheirogaleus medius and provide support for the view that blobs are an evolutionary specialization of primate visual cortex that evolved only once, early in primate history. In other aspects of architectonic organization, area V1 of this Cheirogaleus individual closely resembles that of other strepsirhine primates, such as Galago. We were able to identify additional divisions of cortex in this individual, including the middle temporal visual area (MT), auditory cortex, and the primary somatosensory area (S1 or area 3b). These observations indicate that valuable neuroanatomical information can, in favorable cases, be obtained from rare mammalian species that die of natural causes in captivity or which must be euthanized, even though the animals have not been perfused.

Animals↗

Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus).

Environmental factors that regulate the sexual activity of male lesser mouse lemurs have been studied experimentally with more than 60 captive animals over an 8-year period. In this nocturnal Malagasy prosimian, variation in day length is the primary factor controlling seasonal sexual activity. Plasma testosterone concentrations were low (= 9 ng/ml) during short days and reached 60 ng/ml during long days (> 12-hour day). This cyclic pattern persists unchanged when artificial photoperiodic rhythms are applied and is not altered by ageing. The timing of puberty is also regulated by photoperiodic changes. Nevertheless, the sexual activity of the male lesser mouse lemur can be dramatically modified by the social environment. In heterosexual groups, behavioural and physiological components of sexual activity are depressed in all males except the dominant one, whose aggressive interactions are always successful. Intermale sexual inhibition was shown to be mediated by chemical cues present in the urine of dominant or isolated males but not in urine of subordinate individuals. The inhibitory signals possess lipophilic properties and are not contingent on the gonadal activity of the urine donor but are linked to adrenocortical activity. By contrast, chemical signals stimulating the reproductive function of all males are found in the urine of females, the presence of which is required for the establishment of clear dominance among grouped males. Endocrine mechanisms underlying intermale sexual inhibition by chemical cues were analysed. Variations in prolactin strongly suggest that olfaction interacts with the photoperiodic regulation of reproductive function, leading to changes in the sensitivity of the negative feedback effect of testosterone on gonadotrophin secretion. Inhibitory or stimulatory effects of chemical signals are discussed in the context of their functional significance for wild populations.

Aggression↗

Olfactory bulbectomy modifies photic entrainment and circadian rhythms of body temperature and locomotor activity in a nocturnal primate.

Studies on rodents have emphasized that removal of the olfactory bulbs modulates circadian rhythmicity. Using telemetric recordings of both body temperature (Tb) and locomotor activity (LA) in a male nocturnal primate, the gray mouse lemur, the authors investigated the effects of olfactory bulbectomy on (1) the circadian periods of Tb and LA in constant dim light condition, and (2) photic re-entrainment rates of circadian rhythms following 6-h phase shifts of entrained light-dark cycle (LD 12:12). Under free-running condition, bulbectomized males had significantly shorter circadian periods of Tb and LA rhythms than those of control males. However, the profiles of Tb rhythms, characterized by a phase of hypothermia at the beginning of the subjective day, and Tb parameters were not modified by olfactory bulbectomy. Under a light-dark cycle, olfactory bulbectomy significantly modified the expression of daily hypothermia, especially by an increase in the latency to reach minimal daily Tb, suggesting a delayed response to induction of daily hypothermia by light onset. Reentrainment rates following both a 6-h phase advance and a 6-h phase delay of entrained LD were also delayed in bulbectomized males. Olfactory bulbectomy led to significant fragmentation of locomotor activity and increased locomotor activity levels during the resting period. The shortening of circadian periods in bulbectomized males could partly explain the delayed responses to photic stimuli since in control males, the longer the circadian period, the better the response to light entrainment. This experiment shows for the 1st time that olfactory bulbs can markedly modify the circadian system in a primate.

Animals↗

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.

Aging↗