Martine Perret

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.

Change in Photoperiodic Cycle Affects Life Span in a Prosimian Primate (Microcebus murinus

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.

Behavioral thermoregulation in mammals: a review.

In mammals, thermoregulation is a key feature in the maintenance of homeostasis. Thermoregulatory capacities are strongly related to energy balance and animals are constantly seeking to limit the energy costs of normothermia. In case of thermal changes, physiological mechanisms are enhanced, increasing rates of energy expenditure. However, behavioral adjustments are available for species to lower the autonomic work, and thus reduce the energy costs of thermoregulatory responses. Hence, thermogenesis-induced metabolic costs can be reduced during cold exposure, and hyperthermia associated to dehydration can be avoided during heat exposure. Hypothermia avoidance consists in a concomitant decrease in heat dissipation and increase in heat production. Inversely, heat exchange is enhanced and body heat production is reduced when avoiding hyperthermia. The different behavioral strategies available for mammal species to cope with both decreased and increased levels of ambient temperature are reviewed. Moreover, thermoregulation function is under the control of central, metabolic, energetic and endocrine systems, which induces that parameters such as hour of the day, season, gender or aging may affect thermoregulatory adjustments. Some examples will be given.

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.

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 °C to 35 °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 °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 °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.

Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus

Abstract In primates, age determination using lines of arrested growth (LAGs) from bones has rarely been attempted, andthe reliability of these structures has never been experimentally validated. In order to test skeletochronology inprimates, LAGs were studied mainly in the long bones of known age Microcebus murinus , a small primate, whosepotential longevity may reach 12 years. LAGs were extensively studied in 43 males and 23 females ranging fromjuveniles to 11-year-old adults. All individuals were born and reared in captivity. Some young individuals wereinjected with fluorescent dyes to quantify bone growth rates. LAGs in the diaphysis of the tibia are well correlatedwith age and this skeletal element appears to be the best for assessing skeletochronology in Microcebus murinus .There is strong evidence that the seasonal cycle of photoperiodicity is more important than age alone in producingLAGs. Key words : age determination, skeletochronology, primates, Microcebus murinus INTRODUCTION

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 males 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.

Photoperiod-induced changes in energy balance in gray mouse lemurs

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.

Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus murinus)

Energetic benefits provided by sharing a nest were investigated by measuring resting metabolic rate in the lesser mouse lemur ( Microcebus murinus ), a nocturnal solitary primate that usually groups in a nest during its diurnal rest. Resting metabolic rate was measured on 32 individuals maintained either alone or grouped with one, two, or three conspecifics originating from the same social group. In this seasonal breeder, individual resting metabolic rate varied significantly from 1.08 ± 0.03 to 1.47 ± 0.05 ( SE ) ml O2 h™1g™1 for nonbreeding and breeding seasons, respectively. During the breeding season, both sexes reduced their energetic expenditure by 20% when grouped in pairs, and maximal energetic benefit (40%) was achieved when three animals nested together. During the nonbreeding season, maximal energetic gain was observed when as few as two animals nested together because resting metabolic rate was already decreased. Finally, when three or four animals shared the same nest, resting metabolic rate was minimal, independent of sex and season, at 0.88 ml O2 h™1g™1, suggesting that nest-sharing in this solitary primate is an important strategy to minimize energetic costs to cope with seasonal shortage of food.

Influence of social factors on sex ratio at birth, maternal investment and young survival in a prosimian primate

SummaryIn order to determine whether social factors influence sex ratio at birth in lesser mouse lemurs, experiments were conducted during 5 successive breeding periods on 51 females. At the beginning of the breeding season, females were either isolated (I) or grouped (G) in heterosexual groups with an increasing number of females (2, 3 or 4). To ensure mating, I females were introduced in a group only during the oestrous period. After mating, both I and G females were isolated during pregnancy and lactation. Reproductive capacities of females in terms of oestrus occurrences (n = 324), impregnations (n−210), pregnancies (n = 136) or abortions (n = 38) or litter sizes (1–3 young) were affected neither by age and parity of females nor by group housing prior to conception. G females produced significantly more sons than daughters (67% males for 189 newborn) while females living alone except during the mating period demonstrated a significant inverse tendency (39.6% males for 96 newborn). Distribution of sexes in litters was statistically different from random and varied according to the shift of sex ratio at birth. In G females, the shift in the sex ratio towards males was consistent across the different groups, independent of the number of females living together, suggesting that the presence of only 1 female is sufficient to induce a bias in the sex ratio. No correlation was found between infant survival at weaning and age, parity or group housing of the mother. The maternal investment allocated to male or female newborn was similar provided the litter contained at least 1 male. In litters without males, growth and survival of female infants were significantly less. These results on sex ratio bias in captive female mouse lemurs agree with directions of bias predicted by the local resource competition model for facultative sex ratio adjustment (Clark 1978). Nevertheless, the pattern observed in mouse lemurs appears to be independent of the nutritional state of the female and of differential maternal investment.