Skeletal muscle and metabolic flexibility in response to changing energy demands in wild birds

Abstract

Phenotypically plastic responses of animals to adjust to environmental variation are pervasive. Reversible plasticity (i.e., phenotypic flexibility), where adult phenotypes can be reversibly altered according to prevailing environmental conditions, allow for better matching of phenotypes to the environment and can generate fitness benefits but may also be associated with costs that trade-off with capacity for flexibility. Here, we review the literature on avian metabolic and muscle plasticity in response to season, temperature, migration and experimental manipulation of flight costs, and employ an integrative approach to explore the phenotypic flexibility of metabolic rates and skeletal muscle in wild birds. Basal (minimum maintenance metabolic rate) and summit (maximum cold-induced metabolic rate) metabolic rates are flexible traits in birds, typically increasing with increasing energy demands. Because skeletal muscles are important for energy use at the organismal level, especially to maximum rates of energy use during exercise or shivering thermogenesis, we consider flexibility of skeletal muscle at the tissue and ultrastructural levels in response to variations in the thermal environment and in workloads due to flight exercise. We also examine two major muscle remodeling regulatory pathways: myostatin and insulin-like growth factor -1 (IGF-1). Changes in myostatin and IGF-1 pathways are sometimes, but not always, regulated in a manner consistent with metabolic rate and muscle mass flexibility in response to changing energy demands in wild birds, but few studies have examined such variation so additional study is needed to fully understand roles for these pathways in regulating metabolic flexibility in birds. Muscle ultrastrutural variation in terms of muscle fiber diameter and associated myonuclear domain (MND) in birds is plastic and highly responsive to thermal variation and increases in workload, however, only a few studies have examined ultrastructural flexibility in avian muscle. Additionally, the relationship between myostatin, IGF-1, and satellite cell (SC) proliferation as it relates to avian muscle flexibility has not been addressed in birds and represents a promising avenue for future study.

Gene expression shifts in Emperor penguin adaptation to the extreme Antarctic environment

“…Although the muscle is a highly specialised tissue, the signatures of gene expression were not limited to a narrow set of genes or processes involved only in the structural organisation of muscle fibres. Instead, our findings are consistent with the crucial role played by the muscle in temperature homeostasis and whole body energy metabolism (Swanson et al, 2022).…”

A multi-isotope approach reveals seasonal variation in the reliance on marine resources, production of metabolic water, and ingestion of seawater by two species of coastal passerine to maintain water balance

“…Under such a scenario, the contribution of metabolic water to the body water pool would decrease. Our results contrast with the typical acclimatization response of birds from higher latitudes (McKechnie et al, 2015;Noakes and McKechnie, 2020;Swanson et al, 2022) and supports the idea that changes in BMR is not related to enhancing cold tolerance in areas where birds face milder winter minimum temperatures and more modest thermoregulatory demands.…”

Editorial: Avian behavioral and physiological responses to challenging thermal environments and extreme weather events

“…In addition to changes in average temperatures, however, global change is predicted to increase climate variability, with more frequent extreme events for many locations (Jentsch et al, 2007;Wallace et al, 2014;Cohen et al, 2018). Increasing extreme summer maximum temperatures and more variable winter temperatures can have negative consequences for birds, including mass mortality events (McKechnie and Wolf, 2010;McKechnie et al, 2021b), phenotype-environment mismatches (Boyles et al, 2011;Jimenez et al, 2020;Vézina et al, 2020;Ruuskanen et al, 2021), reduced reproductive capacities (Carroll et al, 2018;Nord and Nilsson, 2019;van de Ven et al, 2020), and altered offspring physiology and behavior (Mariette and Buchanan, 2016;Mariette, 2020). Future research incorporating not only behavior and physiology, but also flexibility in these traits and their thermal reaction norms, into population and distribution models will be critical to understand impacts of climate change on avian biodiversity.…”

“…Metabolic flexibility allows birds to match metabolic rates to environmental conditions (Swanson, 2010). Underlying mechanisms of metabolic flexibility include adjustments in muscle size (Swanson and Vézina, 2015;Swanson et al, 2022) and cellular aerobic and fat catabolism capacities (Swanson, 2010), but the contribution of other metabolic pathways to this flexibility is poorly known (Stager et al, 2015;Cheviron and Swanson, 2017). Wone and Swanson used integrated metabolomics/transcriptomics analyses to document seasonal changes in amino acid, lipid-and cellular metabolism pathways in two passerine birds and identified a potential role for nicotinamide-adenine-nucleotide derivatives in regulating cellular metabolism.…”

“…It is this combination of behavioral and physiological responses at multiple levels of organization that determines the survival probability of birds in thermally challenging situations (e.g., Albright et al, 2017;Petit et al, 2017). Moreover, thermal conditions experienced during reproduction can affect parental investment and nestling development, with potentially longterm consequences (Nord and Giroud, 2020;van de et al, 2020;Broggi et al, 2022). Our knowledge of response mechanisms, their time courses, and their impacts on fitness, however, remains incomplete.…”