Advertisement

Preparing to migrate: expression of androgen signaling molecules and insulin-like growth factor-1 in skeletal muscles of Gambel’s white-crowned sparrows

  • Devaleena S. Pradhan
  • Chunqi Ma
  • Barney A. Schlinger
  • Kiran K. Soma
  • Marilyn Ramenofsky
Original paper

Abstract

Migratory birds, including Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii), exhibit profound modifications of skeletal muscles prior to migration, notably hypertrophy of the pectoralis muscle required for powered flight. Muscle growth may be influenced by anabolic effects of androgens; however, prior to spring departure, circulating androgens are low in sparrows. A seasonal increase in local androgen signaling may occur within muscle to promote remodeling. We measured morphological parameters, plasma and tissue levels of testosterone, as well as mRNA expression levels of androgen receptor, 5α-reductase (converts testosterone to 5α-dihydrotestosterone), and the androgen-dependent myotrophic factor insulin-like growth factor-1. We studied the pectoralis muscle as well as the gastrocnemius (leg) muscle of male sparrows across three stages on the wintering grounds: winter (February), pre-nuptial molt (March), and pre-departure (April). Testosterone levels were low, but detectable, in plasma and muscles at all three stages. Androgen receptor mRNA and 5α-reductase Type 1 mRNA increased at pre-departure, but did so in both muscles. Notably, mRNA levels of insulin-like growth factor-1, an androgen-dependent gene critical for muscle remodeling, increased at pre-departure in the pectoralis but decreased in the gastrocnemius. Taken together, these data suggest a site-specific molecular basis for muscle remodeling that may serve to enable long-distance flight.

Keywords

5α-Reductase Androgen receptor Life-history stages Songbird Testosterone 

Abbreviations

5α-DHT

5α-Dihydrotestosterone

AR

Androgen receptor

GAPDH

Glyceraldehyde-3-phophate dehydrogenase

IGF-1

Insulin-like growth factor-1, IGF-1

T

Testosterone

Notes

Acknowledgements

We thank E. Graves, Drs. Z. Németh, J. Krause, and J. Pérez for help with fieldwork, D. Comito and R. Van Ness for help with laboratory assays, and Drs. X. Chen and M. Rensel for technical advice. This study was supported by The National Institutes of Health T32 training grant (5T32HD007228) to DSP, National Science Foundation ARC-1147289 to MR, Canadian Institutes of Health Research Operating Grant MOP 133606 to KKS, and National Institutes of Health MH061994 to BAS. All authors contributed to the writing of the manuscript. DSP performed the molecular laboratory work and associated data analysis. CM performed T measurements and participated in data analysis. BAS and KKS participated in the design of the study and provided technical advice. MR conceived of the study, designed the study, coordinated the study, collected field data, participated in morphological data analysis. All authors gave final approval for publication. All applicable international, national, and University of California Davis Institutional Animal Care and Use Committee (IACUC—Protocol #17144) guidelines were followed and conducted under the scientific collecting permits of M. Ramenofsky issued by the California Department of Fish and Wildlife (# 11024) and US Fish and Wildlife Department (# MB11826A-5).

Compliance with ethical standards

Conflict of interest

Authors have no competing or conflict of interests.

References

  1. Aizawa K, Iemitsu M, Maeda S, Otsuki T, Sato K, Ushida T, Mesaki N, Akimoto T (2010) Acute exercise activates local bioactive androgen metabolism in skeletal muscle. Steroids 75:219–223CrossRefPubMedGoogle Scholar
  2. Bailey DJ, Ma C, Soma KK, Saldanha CJ (2013) Inhibition of hippocampal aromatization impairs spatial memory performance in a male songbird. Endocrinology 154:4707–4714CrossRefPubMedPubMedCentralGoogle Scholar
  3. Battley PF, Piersma T (1997) Body composition of lesser knots (Calidris canutus rogersi) preparing to take off on migration from northern New Zealand. Notornis 44:137–150Google Scholar
  4. 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 147:266–273CrossRefGoogle Scholar
  5. Bauchinger U, Both C, Piersma T (2005) Are there specific adaptations for long-distance migration in birds? The search for adaptive syndromes. Ann NY Acad Sci 1046:214–215CrossRefPubMedGoogle Scholar
  6. Baulieu E-E, Robel P (1998) Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids. Proc Natl Acad Sci USA 95:4089–4091CrossRefPubMedGoogle Scholar
  7. Biewener AA (2011) Muscle function in avian flight: achieving power and control. Philos Trans R Soc London B 366:1496–1506CrossRefGoogle Scholar
  8. Blanchard BD (1941) The white-crowned sparrows (Zonotrichia leucophrys) of the Pacific seaboard: environment and annual cycle. Univ Calif Publ Zool 46:1–176Google Scholar
  9. Boonstra R, Mo K, Monks DA (2014) Managing anabolic steroids in pre-hibernating arctic ground squirrels: obtaining their benefits and avoiding their costs. Biol Lett 10:20140734–20140734CrossRefPubMedPubMedCentralGoogle Scholar
  10. Boswell T, Richardson RD, Seeley RJ, Ramenofsky M, Wingfield JC, Friedman MI, Woods SC (1995) Regulation of food intake by metabolic fuels in white-crowned sparrows. Am J Physiol Regul Integr Comp Physiol 269:R1462–R1468CrossRefGoogle Scholar
  11. Canoine V, Fusani L, Schlinger B, Hau M (2007) Low sex steroids, high steroid receptors: increasing the sensitivity of the nonreproductive brain. J Neurobiol 67:57–67CrossRefGoogle Scholar
  12. Carson JA, Manolagas SC (2015) Effects of sex steroids on bones and muscles: similarities, parallels, and putative interactions in health and disease. Bone 80:67–78CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chambon C, Duteil D, Vignaud A, Ferry A, Messaddeq N, Malivindi R, Kato S, Chambon P, Metzger D (2010) Myocytic androgen receptor controls the strength but not the mass of limb muscles. Proc Natl Acad Sci USA 107:14327–14332CrossRefPubMedGoogle Scholar
  14. Cornelius JM, Boswell T, Jenni-Eiermann S, Breuner CW, Ramenofsky M (2013) Contributions of endocrinology to the migration life history of birds. Gen Comp Endocrinol 190:47–60CrossRefPubMedGoogle Scholar
  15. Dietz MW, Piersma T, Dekinga A (1999) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J Exp Biol 202:2831–2837PubMedGoogle Scholar
  16. Dolnik VR, Blyumental TI (1967) Autumnal premigratory and migratory periods in the chaffinch (Fringilla coelebs coelebs) and some other temperate-zone passerine birds. Condor 69:435–468CrossRefGoogle Scholar
  17. Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608CrossRefGoogle Scholar
  18. Dubois V, Laurent M, Boonen S, Vanderschueren D, Claessens F (2011) Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions. Cell Mol Life Sci 69:1651–1667CrossRefPubMedGoogle Scholar
  19. Eaton J, Pradhan DS, Barske J, Fusani L, Canoine V, Schlinger BA (2018) 3β-HSD expression in the CNS of a manakin and finch. Gen Comp Endocrinol 256:43–49CrossRefPubMedGoogle Scholar
  20. Edwards CL (1886) The relation of the pectoral muscles of birds to the power of flight. Amer Nat 20:25–29CrossRefGoogle Scholar
  21. Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scand 23:238–243CrossRefGoogle Scholar
  22. Feng NY, Katz A, Day LB, Barkse J, Schlinger BA (2010) Limb muscles are androgen targets in an acrobatic tropical bird. Endocrinology 151:1042–1049CrossRefPubMedGoogle Scholar
  23. Fokidis HB, Prior NH, Soma KK (2013) Fasting increases aggression and differentially modulates local and systemic steroid levels in male zebra finches. Endocrinology 154:4328–4339CrossRefPubMedGoogle Scholar
  24. Fraley GS, Steiner RA, Lent KL, Brenowitz EA (2010) Seasonal changes in androgen receptor mRNA in the brain of the white-crowned sparrow. Gen Comp Endocrinol 166:66–71CrossRefPubMedGoogle Scholar
  25. Fry CH, Ferguson-Lees IJ, Dowsett RJ (1972) Flight muscle hypertrophy and ecophysiological variation of yellow wagtail Motacilla flava races at Lake Chad. J Zool Lond 167:293–306CrossRefGoogle Scholar
  26. Fusani L, Day LB, Canoine V, Reinemann D, Hernandez E, Schlinger BA (2007) Androgen and the elaborate courtship behavior of a tropical lekking bird. Horm Behav 51:62–68CrossRefPubMedGoogle Scholar
  27. Fuxjager MJ, Schultz JD, Barske J, Feng NY, Fusani L, Mirzatoni A, Day LB, Hau M, Schlinger BA (2012) Spinal motor and sensory neurons are androgen targets in an acrobatic bird. Endocrinology 153:3780–3791CrossRefPubMedPubMedCentralGoogle Scholar
  28. Fuxjager MJ, Longpre KM, Chew JG, Fusani L, Schlinger BA (2013) Peripheral androgen receptors sustain the acrobatics and fine motor skill of elaborate male courtship. Endocrinology 154:3168–3177CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fuxjager MJ, Eaton J, Lindsay WR, Salwiczek LH, Rensel MA, Barske J, Sorenson L, Day LB, Schlinger BA (2015) Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor - but not oestrogen receptor—in the forelimb musculature. Funct Ecol 29:1197–1208CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fuxjager MJ, Lee J-H, Chan T-M, Bahn JH, Chew JG, Xiao X, Schlinger BA (2016a) Hormones, genes and athleticism: effect of androgens on the avian muscular transcriptome. Mol Endocrinol 30:254–271CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fuxjager MJ, Schuppe ER, Hoang J, Chew J, Shah M, Schlinger BA (2016b) Expression of 5α- and 5β-reductase in spinal cord and muscle of birds with different courtship repertoires. Front Zool 13:25CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fuxjager MJ, Miles MC, Goller F, Peterson J, Yancey J (2017) Androgens support male acrobatic courtship behavior by enhancing muscle speed and easing the severity of its tradeoff with force. Endocrinology 158:4038–4046CrossRefPubMedGoogle Scholar
  33. Gaunt AS, Hikida RS, Jehl JR Jr, Fenbert L (1990) Rapid atrophy and hypertrophy of an avian flight muscle. Auk 107:649–659CrossRefGoogle Scholar
  34. Grinspoon S, Corcoran C, Lee K, Burrows B, Hubbard J, Katznelson L, Walsh M, Guccione A, Cannan J, Heller H, Basgoz N, Klibanski A (1996) Loss of lean body and muscle mass correlates with androgen levels in hypogonadal men with acquired immunodeficiency syndrome and wasting. J Clin Endocrinol Metab 81:4051–4058PubMedGoogle Scholar
  35. Gwinner E (1990) Circannual rhythms in bird migration: control of temporal patterns and interactions with photoperiod. Springer, BerlinGoogle Scholar
  36. Heimovics SA, Prior NH, Ma C, Soma KK (2016) Rapid effects of an aggressive interaction on dehydroepiandrosterone, testosterone and oestradiol levels in the male song sparrow brain: a seasonal comparison. J Neuroendocrinol 28:1–10CrossRefGoogle Scholar
  37. Herbst KL, Bhasin S (2004) Testosterone action on skeletal muscle. Curr Opin Clin Nutr Metab Care 7:271–277CrossRefPubMedGoogle Scholar
  38. Jehl JR Jr (1997) Cyclical changes in body composition in the annual cycle and migration of the eared grebe Podiceps nigricollis. J Avian Biol 28:132–142CrossRefGoogle Scholar
  39. Kadi F (2008) Cellular and molecular mechanisms responsible for the action of testosterone on human skeletal muscle. A basis for illegal performance enhancement. Brit J Pharmacol 154:522–528CrossRefGoogle Scholar
  40. King JR, Farner DS (1963) The relationship of fat deposition to zugunruhe and migration. Condor 65:200–223CrossRefGoogle Scholar
  41. Lofts B, Marshall AJ (1960) The experimental regulation of zugunruhe and the sexual cycle in the brambling Fringilla montifringilla. Ibis 102:209–214CrossRefGoogle Scholar
  42. Maddison CJ, Anderson RC, Prior NH, Taves MD, Soma KK (2012) Soft song during aggressive interactions: seasonal changes and endocrine correlates in song sparrows. Horm Behav 62:455–463CrossRefPubMedGoogle Scholar
  43. Marsh RL (1984) Adaptations of the gray catbird Dumetella carolinensis to long-distance migration: flight muscle hypertrophy associated with elevated body mass. Physiol Zool 57:105–117CrossRefGoogle Scholar
  44. Overk CR, Perez SE, Ma C, Taves MD, Soma KK, Mufson EJ (2013) Sex steroid levels and AD-like pathology in 3xTgAD Mice. J Neuroendocrinol 25:131–144CrossRefPubMedPubMedCentralGoogle Scholar
  45. Piersma T, van Gils JA (2010) The flexible phenotype: a body-centred integration of ecology, physiology, and behavior. Oxford University Press, OxfordGoogle Scholar
  46. Pradhan DS, Newman AEM, Wacker DW, Wingfield JC, Schlinger BA, Soma KK (2010) Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm Behav 57:381–389CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pradhan DS, Solomon-Lane TK, Grober MS (2015) Contextual modulation of social and endocrine correlates of fitness: insights from the life history of a sex changing fish. Front Neurosci 9:1CrossRefGoogle Scholar
  48. 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 214:2823–2831CrossRefPubMedGoogle Scholar
  49. Ramenofsky M (1990) Fat Storage and Fat Metabolism in Relation to Migration. In: Gwinner E (ed) Bird Migration. Springer, BerlinGoogle Scholar
  50. Ramenofsky M, Németh Z (2014) Regulatory mechanisms for the development of the migratory phenotype: roles for photoperiod and the gonad. Horm Behav 66:148–158CrossRefPubMedGoogle Scholar
  51. Ramenofsky M, Wingfield JC (2007) Regulation of migration. Bioscience 57:165–174CrossRefGoogle Scholar
  52. Ramenofsky M, Agatsuma R, Ramfar T (2008) Environmental conditions affect the behavior of captive, migratory white-crowned sparrows. Condor 110:658–671CrossRefGoogle Scholar
  53. Ramenofsky M, Cornelius JM, Helm B (2012) Physiological and behavioral responses of migrants to environmental cues. J Ornithol 153:S181–S191CrossRefGoogle Scholar
  54. Ramenofsky M, Campion AW, Pérez JH, Krause JS, Nemeth Z (2017) Behavioral and physiological traits of migrant and resident white-crowned sparrows: a common garden approach. J Exp Biol 220:1330–1340CrossRefPubMedGoogle Scholar
  55. Rensel MA, Ding JA, Pradhan DS, Schlinger BA (2018) 11β-HSD types 1 and 2 in the songbird brain. Front Endocrinol 9:86CrossRefGoogle Scholar
  56. Schlinger BA, Brenowitz EA (2017) Neural and hormonal control of birdsong. In: Hormones, brain and behavior, 3rd edn. Academic Press, Oxford, pp 255–290CrossRefGoogle Scholar
  57. Schmidt KL, Pradhan DS, Shah AH, Charlier TD, Chin EH, Soma KK (2008) Neurosteroids, immunosteroids, and the balkanization of endocrinology. Gen Comp Endocrinol 157:266–274CrossRefPubMedGoogle Scholar
  58. Schuppe ER, Pradhan DS, Thonkulpitak K, Drilling C, Black M, Grober MS (2017) Sex differences in neuromuscular androgen receptor expression and sociosexual behavior in a sex changing fish. PLoS One 12:e0177711–e0177713CrossRefPubMedPubMedCentralGoogle Scholar
  59. Schwabl H, Farner DS (1989) Dependency on testosterone of photoperiodically-induced vernal fat deposition in female white-crowned sparrows. Condor 91:108–112CrossRefGoogle Scholar
  60. Soma KK, Hartman VN, Wingfield JC, Brenowitz EA (1999) Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J Comp Neurol 409:224–236CrossRefPubMedGoogle Scholar
  61. Soma KK, Schlinger BA, Wingfield JC, Saldanha CJ (2003) Brain aromatase, 5α-reductase, and 5β-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J Neurobiol 56:209–221CrossRefPubMedGoogle Scholar
  62. Taves MD, Ma C, Heimovics SA, Saldanha CJ, Soma KK (2011) Measurement of steroid concentrations in brain tissue: methodological considerations. Front Endocrinol 2:1–13CrossRefGoogle Scholar
  63. Velloso CP (2008) Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol 154:557–568CrossRefPubMedPubMedCentralGoogle Scholar
  64. Velten BP, Welch KC Jr, Ramenofsky M (2016) Altered expression of pectoral myosin heavy chain isoforms corresponds to migration status in the white-crowned sparrow (Zonotrichia leucophrys gambelii). R Soc Open Sci 3:160775CrossRefPubMedPubMedCentralGoogle Scholar
  65. Vézina F, Jalvingh KM, Dekinga A, Piersma T (2007) Thermogenic side effects to migratory predisposition in shorebirds. Am J Physiol Regul Integr Comp Physiol 292:R1287–R1297CrossRefPubMedGoogle Scholar
  66. Wingfield JC (2008) Comparative endocrinology, environment and global change. Gen Comp Endocrinol 157:207–216CrossRefPubMedGoogle Scholar
  67. Wingfield JC, Farner DS (1978) The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol Reprod 19:1046–1056CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Integrative Biology and PhysiologyUniversity of CaliforniaLos AngelesUSA
  2. 2.Laboratory for NeuroendocrinologyUniversity of CaliforniaLos AngelesUSA
  3. 3.Department of PsychologyUniversity of British ColumbiaVancouverCanada
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaLos AngelesUSA
  5. 5.Djavad Mowafaghian Centre for Brain HealthUniversity of British ColumbiaVancouverCanada
  6. 6.Department of Neurobiology Physiology BehaviorUniversity of CaliforniaDavisUSA
  7. 7.Department of Biological SciencesIdaho State UniversityPocatelloUSA

Personalised recommendations