Migration- and exercise-induced changes to flight muscle size in migratory birds and association withIGF1andmyostatinmRNA expression

Abstract

SUMMARYSeasonal adjustments to muscle size in migratory birds may result from preparatory physiological changes or responses to changed workloads. The mechanisms controlling these changes in size are poorly understood. We investigated some potential mediators of flight muscle size (myostatin and insulin-like growth factor, IGF1) in pectoralis muscles of wild wintering or migrating white-throated sparrows (Zonotrichia albicollis), captive white-throated sparrows that were photoperiod manipulated to be in a 'wintering' or 'migratory' (Zugunruhe) state, and captive European starlings (Sturnus vulgaris) that were either exercised for 2 weeks in a wind tunnel or untrained. Flight muscle size increased in photo-stimulated 'migrants' and in exercised starlings. Acute exercise but not long-term training caused increased expression of IGF1, but neither caused a change in expression of myostatin or its metalloprotease activator TLL1. Photo-stimulated 'migrant' sparrows demonstrated increased expression of both myostatin and IGF1, but wild sparrows exhibited no significant seasonal changes in expression of either myostatin or IGF1. Additionally, in both study species we describe several splice variants of myostatin that are shared with distantly related bird species. We demonstrate that their expression patterns are not different from those of the typical myostatin, suggesting that they have no functional importance and may be mistakes of the splicing machinery. We conclude that IGF1 is likely to be an important mediator of muscle phenotypic flexibility during acute exercise and during endogenous, seasonal preparation for migration. The role of myostatin is less clear, but its paradoxical increase in photo-stimulated 'migrants' may indicate a role in seasonal adjustments of protein turnover.

Cross-training in birds: cold and exercise training produce similar changes in maximal metabolic output, muscle masses and myostatin expression in house sparrows,Passer domesticus

“…The reduced pectoralis myostatin protein levels with increased energy demands for both training groups is generally consistent with trends in myostatin expression during winter acclimatization in small birds, including house sparrows (Swanson et al, 2009. However, reduced pectoralis myostatin mRNA and TLL expression has not been previously documented during migration, although pectoralis myostatin protein levels may decrease in the migratory state (Price et al, 2011;King et al, 2015).…”

“…Myostatin is secreted as an inactive latent form that requires cleavage by metalloproteinases, including the tolloid-like proteins TLL-1 and TLL-2, to produce the active C-terminal dimer (Huet et al, 2001;Wolfman et al, 2003). Several studies have examined variation in expression of myostatin and the TLL proteins in birds during periods (migration and winter acclimatization) that cause variation in muscle mass (Swanson et al, 2009Price et al, 2011;King et al, 2015). These studies offer variable support for a role for myostatin in regulating flexible muscle masses throughout the annual cycle in birds, with some finding negative relationships between expression of myostatin and the TLLs and M pec (Swanson et al, 2009), others finding no or positive relationships (Price et al, 2011) and still others finding different trends for mRNA and protein levels King et al, 2015).…”

“…Several studies have examined variation in expression of myostatin and the TLL proteins in birds during periods (migration and winter acclimatization) that cause variation in muscle mass (Swanson et al, 2009Price et al, 2011;King et al, 2015). These studies offer variable support for a role for myostatin in regulating flexible muscle masses throughout the annual cycle in birds, with some finding negative relationships between expression of myostatin and the TLLs and M pec (Swanson et al, 2009), others finding no or positive relationships (Price et al, 2011) and still others finding different trends for mRNA and protein levels King et al, 2015). Nevertheless, the negative relationships among skeletal muscle masses and myostatin or TLL expression for some species, including the focal species for this study, house sparrows Passer domesticus (Swanson et al, 2009), are consistent with a role for myostatin in mediating metabolic flexibility in these species.…”

Regulatory mechanisms of metabolic flexibility in the dark-eyed junco (Junco hyemalis)

“…Guernec et al, 2003), but their role in seasonal regulation of avian adult muscle size is unclear. Swanson et al (2009Swanson et al ( , 2014b found that increases in pectoralis size of wintering passerine birds were associated with decreased expression of MSTN or its metalloproteinase activators (TLL-1, TLL-2), but increases in flight muscle size of photo-stimulated white-throated sparrows (Zonotrichia albicollis) were conflictingly accompanied by increased expression of both IGF1 and MSTN (Price et al, 2011). Although IGF1 expression was not detected in our dataset, MSTN expression did not differ significantly among either temperature or photoperiod treatments.…”

Does immune suppression during stress occur to promote physical performance?

“…Captivity was expected to have weak but negative effects on these traits because: (1) birds would be able to exercise little in cages [and thus experience atrophy due to disuse (Portugal et al, 2009;Price et al, 2011)], and (2) chronically elevated CORT tends to degrade muscle in domesticated game birds (Dong et al, 2007;Hull et al, 2007) and wild songbirds (Awerman and Romero, 2010; Busch et al, 2008;Gray et al, 1990). As our study was not designed to determine how captivity altered muscle growth and viability in sparrows on the molecular level, we can only speculate as to why house sparrow physical performance improved with captivity duration.…”