Abstract
During moderate calorie restriction (CR) the heterotherm Microcebus murinus is able to maintain a stable energy balance whatever the season, even if only wintering animals enter into torpor. To understand its energy saving strategies to respond to food shortages, we assessed protein and energy metabolisms associated with wintering torpor expression or summering torpor avoidance. We investigated body composition, whole body protein turnover, and daily energy expenditure (DEE), during a graded (40 and 80%) 35-day CR in short-days (winter; SD40 and SD80, respectively) and long-days (summer; LD40 and LD80, respectively) acclimated animals. LD40 animals showed no change in fat mass (FM) but a 12% fat free mass (FFM) reduction. Protein balance being positive after CR, the FFM loss was early and rapid. The 25% DEE reduction, in LD40 group was mainly explained by FFM changes. LD80 animals showed a steady body mass loss and were excluded from the CR trial at day 22, reaching a survival-threatened body mass. No data were available for this group. SD40 animals significantly decreased their FM level by 21%, but maintained FFM. Protein sparing was achieved through a 35 and 39% decrease in protein synthesis and catabolism (protein turnover), respectively, overall maintaining nitrogen balance. The 21% reduction in energy requirement was explained by the 30% nitrogen flux drop but also by torpor as DEE FFM-adjusted remained 13% lower compared to ad-libitum. SD80 animals were unable to maintain energy and nitrogen balances, losing both FM and FFM. Thus summering mouse lemurs equilibrate energy balance by a rapid loss of active metabolic mass without using torpor, whereas wintering animals spare protein and energy through increased torpor expression. Both strategies have direct fitness implication: 1) to maintain activities at a lower body size during the mating season and 2) to preserve an optimal wintering muscle mass and function.
Highlights
Torpor is associated with a profound reduction of energy expenditure to as little as 3% of the euthermic rates at ambient temperature [1]
We reported that only wintering mouse lemurs increase their torpor propensity, either during moderate (40%) or severe (80%) calorie restriction [18] (Figure 1)
Animals The 34 adult male grey mouse lemurs (Microcebus murinus, Cheirogaleidae, Primates) used in this study were born in the laboratory breeding-colony of Brunoy (UMR7179 CNRS/ MNHN, France; European Institutions Agreement # 962773) from a stock originally caught along the southwestern coast of Madagascar 40 years ago
Summary
Torpor is associated with a profound reduction of energy expenditure to as little as 3% of the euthermic rates at ambient temperature [1]. The fitness advantages of torpor are two-fold. It likely improves survival during periods of food shortage or reproductive rest [2,3] and may increase reproductive success following these periods [4,5]. Energy and water conservation through torpor is likely to be essential for surviving prolonged periods of restricted energy availability. More energy conservation may not necessarily be more advantageous. High rates of metabolism were hypothesized to be beneficial for endotherms when resources are abundant [6]
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