Maternal exercise during pregnancy promotes physical activity in adult offspring

Abstract

Previous rodent studies have shown that maternal voluntary exercise during pregnancy leads to metabolic changes in adult offspring. We set out to test whether maternal voluntary exercise during pregnancy also induces persistent changes in voluntary physical activity in the offspring. Adult C57BL/6J female mice were randomly assigned to be caged with an unlocked (U) or locked (L) running wheel before and during pregnancy. Maternal running behavior was monitored during pregnancy, and body weight, body composition, food intake, energy expenditure, total cage activity, and running wheel activity were measured in the offspring at various ages. U offspring were slightly heavier at birth, but no group differences in body weight or composition were observed at later ages (when mice were caged without access to running wheels). Consistent with our hypothesis, U offspring were more physically active as adults. This effect was observed earlier in female offspring (at sexual maturation). Remarkably, at 300 d of age, U females achieved greater fat loss in response to a 3-wk voluntary exercise program. Our findings show for the first time that maternal physical activity during pregnancy affects the offspring's lifelong propensity for physical activity and may have important implications for combating the worldwide epidemic of physical inactivity and obesity.-Eclarinal, J. D., Zhu, S., Baker, M. S., Piyarathna, D. B., Coarfa, C., Fiorotto, M. L., Waterland, R. A. Maternal exercise during pregnancy promotes physical activity in adult offspring.

Keywords: activity-stat; developmental programming; metabolic imprinting.

Figure 1.

The overall study design.

Figure 2.

Preliminary and experimental data on maternal exercise. A) A 7 d preliminary test was conducted to determine the activity level of the dams. Compared to those not selected, selected dams showed less variation in running distance by the end of the preliminary test. B) Of the dams studied, there was no significant difference in baseline exercise level among those randomized to the U or L groups. P = 0.58. C) Running distances of the U dams were recorded daily during acclimation, mating, pregnancy, birth, and early lactation. [Note that during the mating period (average. 2.0 d), we did not distinguish between male and female running.] Daily running distance decreased over pregnancy and was nearly zero during lactation. D) Average running velocity of U dams was fairly stable during early pregnancy but declined precipitously during the third trimester.

Figure 3.

Group differences in body weight were found only at P1. A) P1 body weight of U pups (n = 6 litters) was higher than that of L pups (n = 8 litters). P = 0.007. Box plots show median (thick line), 25–75th percentiles (box), and 5–95th percentiles (whiskers) of 48 U and 68 L pups; sex was not ascertained. B) There was no group difference in body weight at P21, P60, P120, or P160 (n = 23–41 mice/group per sex at each age). C) There was no group difference in percentage body fat at P160 (n = 23–41 mice/group per sex).

Figure 4.

Food intake, physical activity, and energy expenditure of L and U offspring. A) Active period (lights-off) food intake was slightly higher in U than in L females at P60. The opposite trend at P160 was not statistically significant (Table 1). B) Wheel running distance during the active period was higher in U than in L females at P60 and P160. This effect was observed in males at P160 only. C) U males showed higher cage activity only at P160. In females, overall cage activity was higher in U than L females at P60; at P160, a significant group × time interaction (Table 1) reflected higher activity during the early dark period. Increased cage activity was also observed in U vs. L males, but only at P160. D) Dark-period energy expenditure was slightly higher in U than in L females at P60. (In each panel are shown mean ± sem for 6 mice of each sex per group across 10, 9, and 8 d at P21, P60, and P160, respectively. The same 6 male and 6 female mice per group, each from a different litter, were studied at each age. Overall effect of Group during each 12-h period: *P < 0.05; **P < 0.01; ***P < 0.001. Significance of group × time interactions is listed in Table 1.

Figure 5.

At P300, U females showed a greater reduction in adiposity in response to a voluntary exercise program. Before exercise, U and L females had comparable body composition (% fat). Over a 3 wk period of housing in a cage with a running wheel, the U females achieved a greater reduction in percentage of fat than did the L females (P = 0.03).