Early-Life Effects on Adult Physical Activity: Concepts, Relevance, and Experimental Approaches

Abstract

Locomotion is a defining characteristic of animal life and plays a crucial role in most behaviors. Locomotion involves physical activity, which can have far-reaching effects on physiology and neurobiology, both acutely and chronically. In human populations and in laboratory rodents, higher levels of physical activity are generally associated with positive health outcomes, although excessive exercise can have adverse consequences. Whether and how such relationships occur in wild animals is unknown. Behavioral variation among individuals arises from genetic and environmental factors and their interactions as well as from developmental programming (persistent effects of early-life environment). Although tremendous progress has been made in identifying genetic and environmental influences on individual differences in behavior, early-life effects are not well understood. Early-life effects can in some cases persist across multiple generations following a single exposure and, in principle, may constrain or facilitate the rate of evolution at multiple levels of biological organization. Understanding the mechanisms of such transgenerational effects (e.g., exposure to stress hormones in utero, inherited epigenetic alterations) may prove crucial to explaining unexpected and/or sex-specific responses to selection as well as limits to adaptation. One area receiving increased attention is early-life effects on adult physical activity. Correlational data from epidemiological studies suggest that early-life nutritional stress can (adversely) affect adult human activity levels and associated physiological traits (e.g., body composition, metabolic health). The few existing studies of laboratory rodents demonstrate that both maternal and early-life exercise can affect adult levels of physical activity and related phenotypes. Going forward, rodents offer many opportunities for experimental studies of (multigenerational) early-life effects, including studies that use maternal exposures and cross-fostering designs.

Keywords: activitystat; developmental programming; epigenetics; exercise; genotype-by-environment interaction; metabolic imprinting; obesity; wheel running.

Figure 1.

Illustration of genetic, environmental, and epigenetic factors acting at various stages of an organism’s life history. (For simplicity, genotype-by-environment interactions are not depicted.) Epigenetic mechanisms are one of several developmental processes that are influenced by environment, especially during so-called critical periods (Waterland and Garza 1999). Mechanisms of epigenetic effects, which alter gene expression without changing DNA sequences, include DNA methylation and histone modification. “Ontogeny” can be used to describe the entire sequence from fertilization (conception) through development, growth, sexual maturation, aging, and senescence. Additional genes (not shown) may act not only at specific ages or stages but generally across most or all of ontogeny. Similarly, some environmental factors (e.g., pH of a lake in which fish live) may last for the entire lifecycle (subject to seasonal cycles). For many animals, immediate maternal environmental effects stop at weaning (e.g., for mice in a lab setting), but this is not necessarily the case for humans of for other animals in the wild, especially for species in which offspring tend to inherit their parents’ home ranges or territories.

Figure 2.

Potential experimental design to elucidate early-life effects on adult phenotypes, as well as possible trans-generational effects. Life-history and developmental stages are based on placental mammals, and specific timing of events is based on house mice. The maternal environment and/or the juvenile environment can be modified in many ways, including through changes in diet or the providing of access to exercise wheels (Acosta et al. 2015). During the post-natal period from birth to weaning, such factors as litter size or ambient temperature could be manipulated, thus providing other avenues of environmental manipulation that do not derive solely and directly from the mother. Cross-fostering designs also have much to offer, as discussed in the text.