Why be thrifty? Sex-specific heterothermic patterns in wintering captive Microcebus murinus do not translate into differences in energy balance

Abstract

SummaryThe physiological mechanisms of the responses toward stressors are the core of ecophysiology studies to understand the limits of an organism’s flexibility and better predict the impact of environmental degradation on natural populations. However, little information is available when we question inter-individual variability of these physiological responses, even though they can be particularly important. Some observations of intersexual differences in heterothermy raised the question of a difference in energy management between sexes. Here we assess male and female differences in a mouse lemur model (Microcebus murinus), a highly seasonal Malagasy primate, studying their physiological flexibility toward caloric restriction, and examining the impact on their reproductive success. These animals are adapted for naturally changing food availability and climate conditions, and can express deep torpor, allowing them to spare their energy expenses over the dry and cold season. We monitored body mass and body temperature on 12 males and 12 females over winter, applying a chronic 40% caloric restriction to 6 individuals of each group. Our results showed variability of Tb modulations throughout winter and in response to caloric treatment depending on the sex, as females entered deep torpor regardless of food restriction, while only CR males had a similar response. The use of deep torpor, however, did not translate into better body condition either in females, or in response to CR, and did not clearly affect reproductive success. The favorable captive context potentially buffered the depth of torpor and minimized the positive effects of using torpor on energy savings. However, our results may emphasize the existence of other benefits of heterothermic responses than fat reserves.

Grey Mouse Lemurs’ response to acute caloric restriction before reproduction supports the “Thrifty Female Hypothesis”

“…It is somehow surprising, considering the present results, that a chronic 40% CR could not discriminate a thriftier phenotype in female grey mouse lemurs (Noiret et al, 2021). In comparison, this 80% intense CR was designed to be considered as an acute stress compared to the CTL ration animals received during their upstream winter in breeding conditions, before the start of the present experiment.…”

“…Moreover, females were described to use deeper and longer torpor bouts than males to face food rarefaction at the onset of winter in field conditions (Vuarin et al, 2015). However, in a previous study in laboratory conditions, even if wintering males and females expressed strong specificities in their thermic profiles, we have not evidenced a difference in energy balance between sexes under either control ration or a 40% caloric restriction (Noiret et al, 2021). We make the hypothesis that the expression of female thrifty phenotype during winter could occur in more energetically-challenging conditions.…”

“…However, we do not know if they anticipate the reproductive season by reactivating their metabolism during late winter as males do, which would tighten the gap in energy expenditure between the two wintering sexes. Indeed, a previous follow up of the effects of a chronic (6 months) and moderate (40%) CR applied in wintering grey mouse lemurs showed that females lost as much BM as CR males during the second half of winter contrary to what was expected, and despite different torpor profiles in response to CR (Noiret et al, 2021). The present study however shows that females Microcebus murinus exhibit thriftier phenotypes than males under more acute and intense conditions during late winter, which conforms with the TFH.…”

“…In contrast to little brown bats, grey mouse lemurs mating takes place during the transition to the wet season in nature (Radespiel et al, 2006), and about 2 weeks after LD initiation in laboratory conditions (Perret and Aujard, 2001). Even if males Microcebus murinus begin spermatogenesis earlier during the second half of winter to prepare for mating (Perret et Aujard 2001, Noiret et al 2021), the expected gap of MR between sexes is not so obvious compared to the little brown bats, as females stay active during the night. Female birds and mammals are known to reactivate their reproductive axis by responding to photoperiodic change when transitioning to summer (Simonneaux and Ribelayga, 2003).…”

Molecular Liver Fingerprint Reflects the Seasonal Physiology of the Grey Mouse Lemur (Microcebus murinus) during Winter

“…Interestingly, female mouse lemurs have a delayed return to reproductive activity compared to males (estrus begin at the photoperiodic transition between winter and summer) and use their fat reserves later on, during gestation and lactation [20]. This temporal difference results in different patterns of seasonal variations in body mass [20] and probably interferes with the response to environmental stress [65,66]. There is, therefore, a high probability that liver remodeling will differ between males and females in winter, which should be investigated.…”