Maternal exercise opportunity before, during, and after pregnancy alters maternal care behavior and offspring development and survival, but has few effects on offspring physical activity or body composition

Abstract

Early-life experiences, especially during critical periods of development and growth, can have long-lasting effects on adult phenotypes. Parents are a crucial part of the offspring early-life environment, particularly in mammals (e.g., via pregnancy), and parental behaviors (e.g., maternal exercise) can modify the early-life environment experienced by offspring. Such changes might be beneficial or detrimental, depending on how they affect offspring development and growth or interact with other key parental behaviors (e.g., nursing). We used mice from a long-term artificial selection experiment for high voluntary wheel-running behavior to determine whether maternal exercise opportunity affected (1) maternal physical activity, (2) maternal care behavior, or (3) offspring physical activity and body composition. Eighty prospective dams (40 from 4 selectively bred High Runner [HR] lines and 40 from 4 non-selected Control [CON] lines) were housed with continuous wheel access starting two weeks prior to breeding and ending 10 days postpartum, after which dams were housed without wheels until offspring weaning (21 days postpartum). An additional 100 dams (50 HR, 50 CON) were housed without wheels. Prospective dams from HR lines ran more revolutions/day (mainly by running faster) than those from CON lines when individually housed and in the days leading up to, but not after, birth. During postpartum days 1-5, HR and CON dams with wheels tended to exhibit less maternal behavior than those without (P_Wheel = 0.0672). During post-partum days 6-10, HR dams with wheels continued to exhibit less maternal behavior than those without, whereas CON dams with wheels exhibited more than those without (P_{Linetype*Wheel} = 0.0218). The proportion of dams giving birth did not differ among groups. However, CON dams with wheels were less likely to have litter death between birth and weaning than those without wheels, whereas the opposite was true for HR dams (P_{Linetype*Wheel} = 0.0447). Both HR and CON dams with wheels had litters with a higher proportion of females at weaning than those without wheels (P_Wheel = 0.0129). Maternal wheel access had few statistically significant effects on offspring, but may have resulted in developmental delays (e.g., delayed eye opening and decreased lean mass at weaning and sexual maturity). Additionally, maternal wheel access and sex may have interacted to affect wheel-running distance (P_Sex*Wheel = 0.0683) and duration (P_Sex*Wheel = 0.0926); female offspring from dams with wheels ran fewer revolutions per day, by running fewer minutes per day, than from dams without wheels, whereas males ran more. However, maternal exercise had no statistically significant effects on offspring food consumption (mass-adjusted), home-cage activity, open-field behavior, the reproductive characteristics of offspring, their adult body composition, nor relative organ masses; nor did maternal wheel access have statistically significant effects on grand-offspring food consumption, body composition or voluntary exercise behavior. Overall, our results provide some support for maternal exercise opportunity altering maternal care behavior. Altered maternal care could explain the observed trends in offspring survival, development, and voluntary exercise behavior. However, these effects did not have apparent long-lasting impacts on offspring or grand-offspring body composition or reproductive characteristics.

Keywords: Maternal care; Parental behavior; Sex differences; Sex ratio; Voluntary exercise; Wheel running.