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.

Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior

“…''Epigenetic'' in modern parlance generally refers to changes caused by modification of gene expression rather than alteration of the genetic code itself. Sometimes the definition is restricted to heritable changes in gene expression that do not involve changes to the underlying DNA sequence, such as may occur by DNA methylation (Waterland and Garza 1999;Burggren and Crews 2014;Waterland 2014;Garland et al 2017) or histone modification (Lennartsson and Ekwall 2009).…”

“…Further support for a negative relationship between circulating leptin levels and physical activity is provided by various studies of humans (e.g., Franks et al 2003;Holtkamp et al 2003: see also Girard et al (2007)). An important area for future research will be determining whether maternal variation in circulating hormone levels is affecting adult phenotypes of their offspring, possibly in a way that contributes to the selection limits observed in all four of the HR lines (Careau et al 2013;Careau et al 2015;Garland et al 2017). …”

“…If so, then correlated responses in other aspects of behavior, life history (Dantzer et al 2017), and organismal performance (e.g., locomotor abilities) should commonly occur because any cell with appropriate receptors could be affected. At the same time, because hormones are likely to affect multiple traits, including through early-life parental effects (e.g., see Garland et al (2017)), they might be ''used'' routinely by selection to achieve (adaptively) correlated changes (Cox et al 2017). Nevertheless, the seminal papers in modern evolutionary physiology scarcely mentioned the endocrine system (Feder 1987;Garland and Carter 1994;Feder et al 2000).…”

Developmental Hypoxia Has Negligible Effects on Long-Term Hypoxia Tolerance and Aerobic Metabolism of Atlantic Salmon (Salmo salar)

“…Developmental plasticity in response to environmental stressors can have long-term consequences for individual performance because of impacts on developmental trajectories (Monaghan 2008;Burggren and Reyna 2011;Mueller et al 2015;Garland et al 2017). For example, a hypoxic developmental rearing environment can impact cardiovascular development and regulation in fish (Pelster 2002;Bagatto 2005;Miller et al 2011).…”

Effects of activity, genetic selection, and their interaction on muscle metabolic capacities and organ masses in mice

“…Koch et al, 2012;Garton et al, 2016) provides a powerful way to examine the evolution of phenotypic plasticity in response to an altered environment. Future studies should also consider both the duration of exercise training and when in the life cycle it occurs, as exposures occurring earlier in life might have greater effects (Garland et al, 2017).…”