Skip to main content
SpringerLink
Log in

Phenotypic flexibility of skeletal muscle and heart masses and expression of myostatin and tolloid-like proteinases in migrating passerine birds

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Migrant birds require large flight muscles and hearts to enhance aerobic capacity and support sustained flight. A potential mechanism for increasing muscle and heart masses during migration in birds is the muscle growth inhibitor myostatin and its metalloproteinase activators, tolloid-like proteinases (TLL-1 and TLL-2). We hypothesized that myostatin, TLL-1 and TLL-2 are downregulated during migration in pectoralis and hearts of migratory passerines to promote hypertrophy. We measured seasonal variation of tissue masses, mRNA expression of myostatin, TLL-1, and TLL-2, and myostatin protein levels in pectoralis muscle and heart for yellow warblers (Setophaga petechia), warbling vireos (Vireo gilvus), and yellow-rumped warblers (Setophaga coronata). Pectoralis mass was greatest in spring for warbling vireos and yellow warblers, but was stable between spring and fall for yellow-rumped warblers. Heart mass was higher in spring than in fall for yellow-rumped warblers, lowest in fall for warbling vireos, and seasonally stable for yellow warblers. Pectoralis and heart mRNA expression of myostatin and the TLLs did not differ significantly for any of the three species, offering little support for our hypothesis for a prominent role for myostatin in regulating migration-induced variation in pectoralis and heart masses. In contrast, pectoralis myostatin protein levels were lowest in spring for all three species, consistent with our hypothesis. Myostatin protein levels in heart, however, were seasonally stable for warbling vireos and yellow warblers, and increased in spring relative to fall for yellow-rumped warblers. These data offer mixed support for our hypothesis for the pectoralis, but suggest that myostatin is not a prominent regulator of migration-induced heart hypertrophy. Moreover, the different seasonal patterns for pectoralis mRNA and protein expression suggest that post-transcriptional modification of myostatin may contribute to pectoralis mass regulation during migration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arendt DH, Smith JP, Bastida CC, Prasad MS, Oliver KD, Eyster KM, Summers TR, Delville Y, Summers CH (2012) Contrasting hippocampal and amygdalar expression of genes related to neural plasticity during escape from social aggression. Physiol Behav 107:670–679

    Article  CAS  PubMed  Google Scholar 

  • Battley PF, Piersma T (1997) Body composition of lesser knots (Calidris canutus rogersi) preparing to take off on migration from northern New Zealand. Notornis 44:137–150

    Google Scholar 

  • Battley PF, Dietz MW, Piersma T, Dekinga A, Tang S, Julsman K (2001) Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting Great Knots. Physiol Biochem Zool 74:435–449

    Article  CAS  PubMed  Google Scholar 

  • Bauchinger U, Biebach H (2006) Transition between moult and migration in a long-distance migratory passerine: organ flexibility in the African wintering area. J Ornithol 147:266–273

    Article  Google Scholar 

  • Bish LT, Morine KJ, Sleeper MM, Sweeney HL (2010) Myostatin is upregulated following stress in an Erk-dependent manner and negatively regulates cardiomyocyte growth in culture and in a mouse model. PLoS ONE 5:e10230

    Article  PubMed Central  PubMed  Google Scholar 

  • Carlisle HA (1998) Abundance, diversity, and energetic condition of Neotropical woodland migrants during stopover in a geographically isolated farmstead woodlot in southeastern South Dakota. M.S. thesis, University of South Dakota, Vermillion

  • Chappell MA, Bech C, Buttemer WA (1999) The relationship of central and peripheral organ masses to aerobic performance variation in House Sparrows. J Exp Biol 202:2269–2279

    PubMed  Google Scholar 

  • Dawson WR, Marsh RL, Yacoe ME (1983) Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol 245:R755–R767

    CAS  PubMed  Google Scholar 

  • Dean KL (1999) Stopover ecology of Neotropical migrant songbirds in riparian corridors in the northern Great Plains. Ph.D. Dissertation, University of South Dakota, Vermillion

  • Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations of pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608

    Article  Google Scholar 

  • Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scand 23:238–243

    Article  Google Scholar 

  • Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345

    Article  PubMed  Google Scholar 

  • Gwinner E (ed) (1990) Bird migration: physiology and ecophysiology. Springer, Berlin

    Google Scholar 

  • Hammond KA, Chappell MA, Cardullo RA, Lin R-I, Johnsen TS (2000) The mechanistic basis of aerobic performance variation in red junglefowl. J Exp Biol 203:2053–2064

    CAS  PubMed  Google Scholar 

  • Helms CW, Drury JHW (1960) Winter and migratory weight and fat field studies on some North American buntings. Bird Band 31:1–40

    Article  Google Scholar 

  • Hittel DS, Berggren JR, Shearer J, Boyle K, Houmard JA (2009) Increased secretion and expression of myostatin in skeletal muscle from extremely obese women. Diabetes 58:30–38

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huet C, Li Z-F, Liu H-Z, Black RA, Galliano M-F, Engvall E (2001) Skeletal muscle cell hypertrophy induced by inhibitors of metalloproteinases; myostatin as a potential mediator. Am J Physiol 281:C1624–C1634

    CAS  Google Scholar 

  • Jehl JR Jr, Henry AE, Swanson DL (2015) Ratios, adaptations, and the differential metabolic capability of avian flight muscles. J Avian Biol 46 (in press)

  • Landys-Ciannelli MM, Piersma T, Jukema J (2003) Strategic size changes of internal organs and muscle tissue in the bar-tailed godwit during fat storage on a spring stopover site. Funct Ecol 17:151–159

    Article  Google Scholar 

  • Lee S-J (2004) Regulation of muscle mass by myostatin. Ann Rev Cell Dev Biol 20:61–86

    Article  CAS  Google Scholar 

  • Liknes ET, Swanson DL (2011) Phenotypic flexibility of body composition associated with seasonal acclimatization of passerine birds. J Therm Biol 36:363–370

    Article  Google Scholar 

  • Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78

    Article  Google Scholar 

  • Liu M, Swanson DL (2014) Physiological evidence that anthropogenic woodlots can substitute for native riparian woodlands as stopover habitat for migrant birds. Physiol Biochem Zool 87:183–195

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103:1744–1751

    Article  CAS  PubMed  Google Scholar 

  • Matsakas A, Friedel A, Hertrampf T, Diel P (2005) Short-term endurance training results in a muscle-specific decrease of myostatin mRNA content in the rat. Acta Physiol Scand 183:299–307

    Article  CAS  PubMed  Google Scholar 

  • Matsakas A, Bozzo C, Cacciani N, Caliaro F, Reggiani C, Mascarello F, Patruno M (2006) Effect of swimming on myostatin expression in white and red gastrocnemius muscle and in cardiac muscle of rats. Exp Physiol 91(6):983–994

    Article  CAS  PubMed  Google Scholar 

  • McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162:1135–1147

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Article  Google Scholar 

  • Petit M, Vézina F (2014) Phenotype manipulations confirm the role of pectoral muscles and haematocrit in avian maximal thermogenic capacity. J Exp Biol 217:824–830

    Article  PubMed  Google Scholar 

  • Petit M, Lewden A, Vézina F (2014) How does flexibility in body composition relate to seasonal changes in metabolic performance in a small passerine wintering at a northern latitude? Physiol Biochem Zool 87:539–549

    Article  PubMed  Google Scholar 

  • Piersma T (1998) Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight? J Avian Biol 29:511–520

    Article  Google Scholar 

  • Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behaviour. Oxford University Press, New York

    Google Scholar 

  • Price ER, Bauchinger U, Zajac DM, Cerasale DJ, McFarlan JT, Gerson AR, McWilliams SR, Guglielmo CG (2011) Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression. J Exp Biol 214:2823–2831

    Article  CAS  PubMed  Google Scholar 

  • Rodgers BD, Garikipati DK (2008) Clinical, agricultural and evolutionary biology of myostatin: a comparative review. Endocr Rev 29:513–534

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruas JL, Whte JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM (2012) A PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151:1319–1331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanchez AMJ, Bernardi H, Py G, Candau RB (2014) Autophagy is essential to support skeletal muscle plasticity in response to endurance exercise. Am J Physiol Regul Integr Comp Physiol 307:R956–R969

    Article  CAS  PubMed  Google Scholar 

  • Swanson DL (1995) Seasonal variation in thermogenic capacity of migratory warbling vireos. Auk 112:870–877

    Article  Google Scholar 

  • Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129

    Google Scholar 

  • Swanson DL, Dean KL (1999) Migration-induced variation in thermogenic capacity in migratory passerines. J Avian Biol 30:245–254

    Article  Google Scholar 

  • Swanson DL, Merkord C (2013) Seasonal phenotypic flexibility of flight muscle size in small birds: a comparison of ultrasonography and tissue mass measurements. J Ornithol 154:119–127

    Article  Google Scholar 

  • Swanson DL, Dean KL, Carlisle HA, Liknes ET (2005) Riparian and woodlot landscape patterns and migration of Neotropical migrants in riparian forests of eastern South Dakota. In: Ralph CJ, Rich TD (eds) Bird conservation implementation and integration in the Americas: proceedings of the third international Partners in Flight conference 2002. Gen Tech Rep PSW-GTR-191, Pacific Southwest Research Station, U.S. Department of Agriculture, Albany, California, pp 541–549

  • Swanson DL, Sabirzhanov B, VandeZande A, Clark TG (2009) Seasonal variation of myostatin gene expression in pectoralis muscle of house sparrows (Passer domesticus) is consistent with a role in regulating thermogenic capacity and cold tolerance. Physiol Biochem Zool 82:121–128

    Article  CAS  PubMed  Google Scholar 

  • Swanson DL, Zhang Y, King MO (2013) Individual variation in thermogenic capacity is correlated with flight muscle size but not cellular metabolic capacity in American goldfinches, Spinus tristis. Physiol Biochem Zool 86:421–431

    Article  PubMed  Google Scholar 

  • Swanson DL, King MO, Harmon E (2014a) Seasonal variation in pectoralis muscle and heart myostatin and tolloid-like proteins in small birds: a regulatory role for seasonal phenotypic flexibility? J Comp Physiol B 184:249–258

    Article  CAS  PubMed  Google Scholar 

  • Swanson DL, Zhang Y, Liu J-S, Merkord CL, King MO (2014b) Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J Exp Biol 217:866–875

    Article  CAS  PubMed  Google Scholar 

  • Swanson DL, Zhang Y, King MO (2014c) Mechanistic drivers of flexibility in summit metabolic rates of small birds. PLoS ONE 9(7):e101577

    Article  PubMed Central  PubMed  Google Scholar 

  • Tallman DT, Swanson DL, Palmer JS (2002) Birds of South Dakota, 3rd edn. South Dakota Ornithologists’ Union, Aberdeen, South Dakota

    Google Scholar 

  • Vézina F, Jalvingh KM, Dekinga A, Piersma T (2006) Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size. J Exp Biol 209:3141–3154

    Article  PubMed  Google Scholar 

  • Vézina F, Jalvingh K, Dekinga A, Piersma T (2007) Thermogenic side effects to migratory disposition in shorebirds. Am J Physiol Regul Integr Comp Physiol 292:R1287–R1297

    Article  PubMed  Google Scholar 

  • Vézina F, Dekinga A, Piersma T (2011) Shorebirds’ seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together. Integr Comp Biol 51:394–408

    Article  PubMed  Google Scholar 

  • Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13:227–232

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomlinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee S-J (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100:15842–15846

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the U.S. National Science Foundation (Grant Number IOS-1021218 to DLS). We thank Tricia Larson, Michelle Harmon, Ming Liu, Kyle Kirby, Stephanie Owens, and Tyler Tordsen for technical assistance in the laboratory and field. We thank Ken Renner, Cathy Beard and John Davidson for access to woodlands for capturing birds. Two anonymous reviewers provided very helpful comments that greatly improved the manuscript and we thank them for their efforts.

Author information

Authors and Affiliations

  1. Department of Biology, University of South Dakota, Vermillion, SD, 57069, USA

    Marisa O. King, Yufeng Zhang, Travis Carter, Jake Johnson, Erin Harmon & David L. Swanson

  2. Sanford Research, Cardiovascular Research Institute, University of South Dakota, Sioux Falls, SD, 57105, USA

    Erin Harmon

Authors
  1. Marisa O. King
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yufeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Travis Carter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jake Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Erin Harmon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David L. Swanson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David L. Swanson.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

King, M.O., Zhang, Y., Carter, T. et al. Phenotypic flexibility of skeletal muscle and heart masses and expression of myostatin and tolloid-like proteinases in migrating passerine birds. J Comp Physiol B 185, 333–342 (2015). https://doi.org/10.1007/s00360-015-0887-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0887-7

Keywords

Search

Navigation