The Skeletal Muscle Response to Energy Deficiency: A Life History Perspective

Abstract

Energy is a finite resource that is competitively distributed among the body's systems and biological processes. During times of scarcity, energetic "trade-offs" may arise if less energy is available than is required to optimally sustain all systems. More immediately essential functions are predicted to be prioritized, even if this necessitates the diversion of energy away from -and potential downregulation of -others. These concepts are encompassed within life history theory, an evolutionary framework with considerable potential to enhance understanding of the evolved biological response to periods of energy deficiency. Skeletal muscle is a particularly interesting tissue to investigate from this perspective, given that it is one of the largest and most energetically costly tissues within the body. It is also highly plastic, responsive to a broad range of stimuli, and contributes to many essential bodily functions, e.g., mechanical, regulatory and storage. These functions may be traded off against each other during periods of energy deficiency, with the nature of the trade-off's dependent on the characteristics of the individual and the circumstances within which the deficit occurs. In this review, we consider the skeletal muscle response to periods of energy deficiency from a life history perspective, along with how this response may be influenced by factors including sex, age, body composition, training and nutritional status.

A Life History Perspective on Athletes with Low Energy Availability

“…The response of muscle to LEA may depend on which of its functions (e.g., mechanical, regulatory or storage) proves to be most immediately essential. This in turn may depend on a host of factors, including sex, life-stage, health and training status, body composition phenotype, the length and severity of LEA, and the macro and micronutrient composition of available energy, as discussed elsewhere [87]. For example, biological sex is thought to influence the muscle response to periods of LEA, with men potentially more susceptible than women to muscle-loss during times of scarcity [88][89][90].…”

Mapping the complexities of Relative Energy Deficiency in Sport (REDs): development of a physiological model by a subgroup of the International Olympic Committee (IOC) Consensus on REDs

“…92 These perspectives reinforce the caveats identified in the updated REDs Conceptual Models, 1 emphasising that LEA and the response to it are not uniform and always negative, [92][93][94] and confirming that the focus should be on problematic LEA exposure. Observations on athletes via the life history lens have included commentary on priorities of energy allocation during energetic stress, noting considerable reliance on the context of both the energy restriction and the individual athlete/environment, [92][93][94] but also the apparent importance of preserving physical capacity. 98 Athletes have allowed a further examination of the constrained energy model of Pontzer and colleagues.…”

“…Aspects of life history theory explain many of the features of the updated REDs Conceptual Models: energy partitioning can occur at different levels and timescales across and within athletes; it can range from transient and reversible, representing a normal and necessary, adaptive response through to more severe impairments to body systems that nevertheless represent survival priorities 92. These perspectives reinforce the caveats identified in the updated REDs Conceptual Models,1 emphasising that LEA and the response to it are not uniform and always negative,92–94 and confirming that the focus should be on problematic LEA exposure. Observations on athletes via the life history lens have included commentary on priorities of energy allocation during energetic stress, noting considerable reliance on the context of both the energy restriction and the individual athlete/environment,92–94 but also the apparent importance of preserving physical capacity 98…”

“…Since then, the evolution of Triad and REDs models has occurred largely via insights gained within sports science/sports medicine research and practice. Only recently have other perspectives on responses to energy mismatches been considered within the sports domain, with forays into evolutionary biology92–94 enabled by recognition that ‘‘nothing in biology makes sense except in the light of evolution” 95. Additionally, anthropologists have developed the reverse interest in athletes as a modern cohort with unique profiles of energy expenditure 60 96 97…”