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.

Keywords: IGF-1; hypertrophy; muscle; myonuclear domain; myostatin.

FIGURE 1

Relationship of variation in pectoralis muscle mass (ΔPectoralis Mass) with variation in summit metabolic rate (ΔM_sum) across a range of natural acclimatization (winter vs. summer in climate with cold or mild winters, migratory vs. non-migratory conditions) and experimental acclimation (cold vs. warm, flight training vs. control) for birds. A linear regression on these data indicated no significant relationship (F _1,17 = 1.918, p = 0.184), including after removal of the “Mild Winters” data point (F _1,16 = 2.775, p = 0.115), suggesting that despite increases in both M_sum and pectoralis muscle mass often occurring under conditions of increasing energy demand in birds, the two traits are not tightly coupled. Data from Swanson (1990), Swanson (1991), Swanson (1995), O’Connor (1995a), O’Connor (1995b), Cooper (2002), Cooper and Swanson (1994), Petit et al. (2014), Liknes and Swanson (2011), Sgueo et al. (2012), Swanson et al. (2014a,, Milbergue et al. (2018), Noakes et al. (2020), DeMoranville et al. (2019), King et al. (2015), Zhang et al. (2015), Vézina et al. (2006).

FIGURE 2

Signaling diagram illustrating myostatin and insulin-like growth factor—1 (IGF-1) pathways. ActRII, activin receptor II; ALK, type I activin receptors; Akt, protein kinase B; PI3K, phosphatidylinositol 3-kinase; TOR, target of rapamycin; TLL, Tolloid-like protein; FOXO, Forkhead Box-O; MURF1, muscle-specific E3 ubiquitin ligase muscle RING-finger 1.

FIGURE 3

A productive model system to study regulation of muscle fiber size as whole-animal energetics change for birds is that of the pectoralis of mourning doves. (A) After fixing the pectoralis muscle in 4% paraformaldehyde, we placed fixed muscle tissue in 25% sucrose for 24 h to cryo-protect the samples. Tissues were then flash frozen in isopentane cooled in liquid nitrogen, mounted at resting length in Optimal Cutting Temperature (O.C.T.) compound and allowed to equilibrate to −19°C in a Leica 1800 cryocut microtome before sectioning. Sections were cut at 30 μm, picked up on slides, air-dried at room temperature, stained with a 250 μg/ml solution of wheat germ agglutinin (WGA) labeled with Alexa Fluor 488 (in green), and 4′,6-diamidino-2-phenylindole (DAPI; in blue), for 30 min, and rinsed in avian ringer’s for 60 min. WGA is a lectin that binds to glycoproteins on the basement membrane of the fiber sarcolemma, and effectively outlines the fiber periphery to allow measurements of fiber size, whereas DAPI irreversibly binds to nuclei. Stained slides were examined with an Olympus Fluoview 1000 laser filter confocal microscope, and pictures were taken at a magnification of ×20. Mourning dove pectoralis muscle contain a population of small muscle fibers with a myonuclear domain (MND) surrounded by a population of large muscle fibers. (B,C) Using data from Jimenez and De Jesus (2021b), we isolated the number of nuclei per fiber and MND of N = 4 mourning doves (N = 135 small fibers and N = 63 large fibers). Using a one-way ANOVA, the small fibers demonstrated a significantly fewer nuclei per mm of fiber (F = 108.83, p < 0.0001; Panel (B), and a significantly smaller MND (F = 27.48, p < 0.001; Panel (C).