The grey mouse lemur uses season-dependent fat or protein sparing strategies to face chronic food restriction

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.

Figure 1. Changes in Torpor frequency in food-deprived mouse lemurs.

Torpor frequency changes during a 5-week food restriction in long-days and short-days mouse lemurs exposed to a 40% food deprivation (LD40 and SD40, respectively) and in short-days 80% calorie restricted animals (SD80) (From Giroud et al. 2009 [61]). Body temperature was recorded by using a small data logger (model TA10TA-F20, 3.2 g; DSI, St Paul, MN), which was implanted in the abdominal cavity of each animal. Torpor was defined when body temperature of mouse lemurs dropped below 33°C. Torpor frequency (0 to 7) represents the number of occurrence of torpor bouts during a week. By using a generalized linear model, we tested the differential time course of torpor frequency over the 5 weeks of food deprivation between the 3 groups of mouse lemurs. In each group, Bonferroni tests compared weeks of food restriction with the control (ad-libitum) value. Values are means ± SE. **p<0.01.

Figure 2. Modifications of body mass and composition in food-restricted mouse lemurs.

Body mass time courses (A) and, changes in fat-free mass (B) and fat mass (C) during 5 weeks of food deprivation. The statistics, mentioned on the right side of the graph, show overall effects of photoperiod (P) and calorie restriction (CRi) on the body mass time courses during a 35-day food deprivation (time) in long-days (LD) and short-days (SD) mouse lemurs under 40% (LD40 and SD40, respectively) and 80% food restriction (LD80 and SD80, respectively). Please, note that LD80 animals were excluded at day 22, before the end of the food-restricted trial. Values are expressed as means ± SE. # LD vs. SD groups under ad-libitum. **p<0.01.

Figure 3. Water turnover changes induced by a 5-week food restriction in mouse lemurs.

LD and SD: long-days and short-days mouse lemurs, respectively. LD40 and SD40: LD and SD animals under a moderate 40% calorie restriction, respectively. SD80: SD mouse lemurs facing a severe 80% food deprivation. Values are means ± SE. **p<0.01 vs. ad-libitum value.

Figure 4. Food-restriction induced changes in energy expenditures in mouse lemurs.

Changes in fat-free mass (FFM)-adjusted daily energy expenditure (DEE, A) and resting metabolic rate (RMR, B) in long-days (LD) and in short-days (SD) mouse lemurs under 40% food restriction (LD40 and SD40, respectively) and SD animals facing an 80% calorie restriction (SD80). Values are means ± SE. *p<0.05, **p<0.01 vs. ad-libitum value.

Figure 5. Changes in nitrogen balance and flux, and protein turnover in food-deprived mouse lemurs.

Changes in mass-specific nitrogen balance (A), nitrogen flux (B), protein synthesis (C) and catabolism (D), normalized by body mass, in long-days (LD) mouse lemurs under a moderate 40% food deprivation (LD40) and in short-days (SD) animals under a 40% or an 80% calorie restriction (SD40 and SD80, respectively). Values are means ± SE. # LD vs. SD groups under ad-libitum. *p<0.05, **p<0.01 vs. ad-libitum value.