Snow buntings preparing for migration increase muscle fiber size and myonuclear domain in parallel with a major gain in fat mass

Abstract

In long‐distance migrants, preparation for migration is typically associated with increases in fat and body mass, and with an enlargement of pectoralis muscle mass that likely improves flight performance. Although changes in muscle mass or size have been well described in migratory birds, potential changes in muscle ultrastructure during this transition still deserves scrutiny. Using outdoor captive snow buntings (Plectrophenax nivalis n = 15) measured during their transition into a spring migratory phenotype as a model system, we studied changes in pectoralis muscle ultrastructure and predicted that muscle fiber diameter could increase in parallel with the gain in body mass. We also expected that larger fibers could either recruit satellite cells to support cellular maintenance and protein turnover, increase myonuclear domain (cytoplasm per nuclei) with a potential increase in protein turnover load per myonucleus, or existing myonuclei could undergo endoreduplication. Buntings increased body mass by 46% within a month, largely due to a > 6‐fold increase in body fat. However, this increase in body mass was also associated with a 36% increase in muscle fiber diameter. Both pectoralis muscle mass (r2 = 0.57–0.77) and fiber diameter (r2 = 0.32) correlated with total body mass, without any change in the number of nuclei per fiber. Consequently, variation in myonuclear domain (i.e. the amount of cytoplasm per nucleus), was also positively associated with body mass (r2 = 0.51). Therefore, buntings preparing for migration may experience an increase in muscle contraction force due to larger muscle fibers, but this is also coupled with increases in myonuclear domain, which may force these cells to increase protein production to safeguard satellite cells.

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

“…More recent studies also generally support the trend of muscle hypertrophy during the migratory period for birds. For example, pectoralis muscle mass and fiber diameter both increased (by approximately 17 and 35%, respectively) with development of migratory condition in outdoor captive Snow buntings (Vézina et al, 2021). Concurrently with this change, myonuclear domain (MND) also increased during migration (Vézina et al, 2021; more on this below).…”

“…For example, pectoralis muscle mass and fiber diameter both increased (by approximately 17 and 35%, respectively) with development of migratory condition in outdoor captive Snow buntings (Vézina et al, 2021). Concurrently with this change, myonuclear domain (MND) also increased during migration (Vézina et al, 2021; more on this below). Velten et al (2016) compared winter flocks of white-crowned sparrows (Zonotrichia leucophrys) in central California with birds just arriving from migration in May in Alaska and found that flight muscle mass was greater upon arrival in Alaska than during winter or just prior to departure in April in California.…”

Short- and long-distance avian migrants differ in exercise endurance but not aerobic capacity

“…Indeed, birds with different migratory strategies substantially differed in muscle fibre diameters and blood capillary density per unit of muscle fibre area [ 23 ] with the latter being highest in long-distance migrants, intermediate in short-distance and lowest in partial/non-migratory populations. Seasonal variation in muscle fibre diameter has recently been found in snow buntings ( Plectrophenax nivalis ) switching from residence to migratory phases, which increases muscle power output while lowering energy costs of muscle maintenance [ 10 ]. Such morphological adjustments are expected to affect rates of fuel and oxygen provision to flight muscles as well as metabolic end-product removal, and consequently, on aerobic endurance.…”

“…Short-and long-distance migrants typically undergo morphological and physiological changes in preparing for migration [4]. They increase lipid storage, pectoral muscle mass [5][6][7], heart mass [8,9], flight muscle fibre volume [10], as well as increases in haematocrit and blood haemoglobin content [11,12]. Along with these morphological modifications, several fatty acid binding proteins are upregulated that facilitate the transfer of fatty acids from the circulation system to myocytes as well as increases in key catabolic enzymes that promote the oxidation of mitochondrial fatty acids [13][14][15][16][17].…”

Flexibility underlies differences in mitochondrial respiratory performance between migratory and non-migratory White-crowned Sparrows (Zonotrichia leucophrys)

“…There is strong evidence that the adaptations that support the energetic demands of avian migration span from whole organism to cellular processes and include an array of fixed 3 , 4 and flexible traits 5 – 7 . Understanding if avian migrants support greater mitochondrial respiratory performance than non-migrants and if those differences are fixed or flexible is a valuable step in understanding the evolution of this fascinating trait.…”