Peripheral androgen receptors sustain the acrobatics and fine motor skill of elaborate male courtship

Endocrinology

Volumn 154, Issue 9, 2013, Pages 3168-3177

  Fuxjager, Matthew J ^a   Longpre, Kristy M ^a   Chew, Jennifer G ^a   Fusani, Leonida ^b   Schlinger, Barney A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF FERRARA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; BICALUTAMIDE;

ACROBATICS; ANIMAL BEHAVIOR; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ARTICLE; BIRD; BODY MOVEMENT; COURTSHIP; MALE; MANACUS VITELLINUS; MOTOR PERFORMANCE; NONHUMAN; PRIORITY JOURNAL;

ANDROGEN RECEPTOR ANTAGONISTS; ANILIDES; ANIMALS; ANIMALS, WILD; AVIAN PROTEINS; DRUG IMPLANTS; FEATHERS; INFUSIONS, SUBCUTANEOUS; MALE; MOTOR SKILLS; MUSCLE, SKELETAL; NITRILES; NONSTEROIDAL ANTI-ANDROGENS; PANAMA; PIGMENTS, BIOLOGICAL; RANDOM ALLOCATION; RECEPTORS, ANDROGEN; RNA, MESSENGER; SEXUAL BEHAVIOR, ANIMAL; SONGBIRDS; TOSYL COMPOUNDS; TREES;

EID: 84883203546     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1302     Document Type: Article

References (57)

1. Hogg JT, Forbes SH. Mating in bighorn sheep: frequent male reproduction via a high-risk "unconventional" tactic. Behav Ecol Sociobiol. 1997;41:33-48.
2. Thorbjarnarson JB, Hernandez G. Reproductive ecology of the Orinoco crocodile (Crocodylus intermedius) in Venezuela. II. Reproductive and social behavior. J Herpetol. 1993;27:371-379.
3. Masonjones HD, Lewis SM. Courtship behavior in the dwarf seahorse, Hippocampus zosterae. Copeia. 1996;634-640.
4. Nuechterlein GL, Storer RW. The pair formation displays of the western grebe. Condor. 1982;84:350-369.
5. Bostwick KS, Prum RO. High-speed video analysis of wing-snapping in two manakin clades (Pipridae: Aves). J Exp Biol. 2003;206: 3693-3706.
6. Frith CB, Cooper WT. Courtship display and mating of Victoria's riflebird, Ptiloris victoriae, with notes on the courtship displays of congeneric species. Emu. 1996;96:102-113.
7. Adkins-Regan E. Hormones and Animal Social Behavior. Princeton, NJ: Princeton University Press; 2005.
8. Regnier M, Herrera AA. Differential sensitivity to androgens within a sexually dimorphic muscle of male frogs (Xenopus laevis). J Neurobiol. 1993;24:1215-1228.
9. Michel G, Baulieu EE. Androgen receptor in rat skeletal muscle: characterization and physiological variations. Endocrinology. 1980;107:2088-2098.
10. Kadi F, Bonnerud P, Eriksson A, Thornell LE. The expression of androgen receptors inhumanneck and limb muscles: effects of training and self-administration of androgenic-anabolic steroids. Histochem Cell Biol. 2000;113:25-29.
11. Rand MN, Breedlove SM. Androgen locally regulates rat bulbocavernosus and levator ani size. J Neurobiol. 1992;23:17-30.
12. Regnier M, Herrera AA. Changes in the contractile properties by androgen hormones in sexually dimorphic muscles of male frogs (Xenopus laevis). J Physiol (Camb). 1993;461:565-581.
13. Brantley RK, Marchaterre MA, Bass AH. Androgen effects on vocal muscle structure in a teleost fish with intersexual and intrasexual dimorphism. J Morphol. 1993;216:305-318.
14. Fischer L, Catz D, Kelley D. An androgen receptor messenger-RNA isoform associated with hormone induced cell proliferation. Proc Nat Acad Sci USA. 1993;90:8254-8258.
15. Veney SL, Wade J. Steroid receptors in the adult zebra finch syrinx: a sex difference in androgen receptor mRNA, minimal expression of estrogen receptor alpha and aromatase. Gen Comp Endocrinol. 2004;136:192-199.
16. Brenowitz EA, Lent K. Act locally and think globally: Intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc Nat Acad Sci USA. 2002;99:12421-12426.
17. Remage-Healey L, Joshi NR. Changing neuroestrogens within the auditory forebrain rapidly transform stimulus selectivity in a downstream sensorimotor nucleus. J Neurosci. 2012;32:8231-8241.
18. Barclay SR, Harding CF. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res. 1990;523:251-262.
19. Soma KK, Wissman AM, Brenowitz EA, Wingfield JC. Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav. 2002;41: 203-212.
20. Schlinger BA, Day LB, Fusani L. Behavior, natural history and neuroendocrinology of a tropical bird. Gen Comp Endocrinol. 2008; 157:254-258.
21. Chapman FM. The courtship of Gould's manakin (Manacus vitellinus vitellinus) on Barro Colorado Island, Canal Zone. BullAmMuseum Nat Hist. 1935;68:472-521.
22. Feng NY, Katz A, Day LB, Barske J, Schlinger BA. Limb muscles are androgen targets in an acrobatic tropical bird. Endocrinology. 2010;151:1042-1049.
23. Fusani L, Day LB, Canoine V, Reinemann D, Hernandez E, Schlinger BA. Androgen and the elaborate courtship behavior of a tropical lekking bird. Horm Behav. 2007;51:62-68.
24. Freeman SN, Mainwaring WIP, Furr BJA. A possible explanation for the peripheral selectivity of a novel non-steroidal pure antiandrogen, Casodex (ICI 176,334). Br J Cancer. 1989;60:664-668.
25. Furr BJA. Casodex (ICI-176,334) - a new, pure, peripherally selective anti-androgen: preclinical studies. Horm Res. 1989;32:69-76.
26. Soma KK, Sullivan K, Tramontin AD, Saldanha CJ, Schlinger BA, Wingfield JC. Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows. J Comp Physiol A. 2000;186:759-769.
27. Fusani L, Gahr M, Hutchison JB. Aromatase inhibition reduces specifically one display of the ring dove courtship behavior. Gen Comp Endocrinol. 2001;122:23-30.
28. Fennell MJ, Radecki SJ, Proudman JA, Scanes CG. The suppressive effects of testosterone on growth in young chickens appears to be mediated via peripheral androgen receptor; studies of the anti-androgen ICI 176,334. Poult Sci. 1996;75:763-766.
29. Sperry TS, Wacker DW, Wingfield JC. The role of androgen receptors in regulating territorial aggression in male song sparrows.Horm Behav. 2010;57:86-95.
30. Day LB, Fusani L, Hernandez E, et al. Testosterone and its effects on courtship in golden-collared manakins (Manacus vitellinus): seasonal, sex, and age differences. Horm Behav. 2007;51:69-76.
31. Day LB, McBroom JT, Schlinger BA. Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus).HormBehav. 2006; 49:223-232.
32. Fuxjager MJ, Schultz JD, Barske J, et al. Spinal motor and sensory neurons are androgen targets in an acrobatic bird. Endocrinology. 2012;153:3780-3791.
33. McDonald JB, Clay RP, Brumfield RT, Braun MJ. Sexual selection on plumage and behavior in an avian hybrid zone: experimental tests of male-male interactions. Evolution. 2001;55:1443-1451.
34. Fuxjager MJ, Barske J, Du S, Day L, Schlinger BA. Androgens regulate gene expression in avian skeletal muscles. PLoS One. 2012; 7:e51482.
35. Tomaszycki ML, Peabody C, Replogle K, Clayton DF, Tempelman RJ, Wade J. Sexual differentiation of the zebra finch song system: potential roles for sex chromosome genes. BMC Neurosci. 2009; 10:24.
36. Harada N, Abedohmae S, Loeffen R, Foidart A, Balthazart J. Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res. 1993;622: 243-256.
37. Wu D, Tang YP, Wade J. Co-localization of Sorting Nexin 2 and androgen receptor in the song system of juvenile zebra finches. Brain Res. 2010;1343:104-111.
38. Lu S, Simon NG, Wang Y, Hu S. Neural androgen receptor regulation: effects of androgen and antiandrogen. J Neurobiol. 1999; 41:505-512.
39. Schlinger BA, Schultz JD, Hertel F. Neuromuscular and endocrine control of an avian courtship behavior.HormBehav. 2001;40:276-280.
40. Fusani L, Giordano M, Day LB, Schlinger BA. High-speed video analysis reveals individual variability in the courtship displays of male golden-collared manakins. Ethology. 2007;113:964-972.
41. Heizmann CW, Berchtold MW, Rowlerson AM. Correlation of parvalbumin concentration with relaxation speed in mammalian muscle. Proc Natl Acad Sci USA. 1982;79:7243-7247.
42. Muntener M, Kaser L, Weber J, Berchtold MW. Increase of skeletal muscle relaxation speed by direct injection of parvalbumin cDNA. Proc Natl Acad Sci USA. 1995;92:6504-6508.
43. Musaro A, McCullagh KJA, Naya FJ, Olson EN, Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature. 1999;400:581-585.
44. Adams GR, McCue SA. Localized infusion of IGF-I results in skeletal muscle hypertrophy. J Appl Physiol. 1998;84:1716-1722.
45. Kaspar BK, Llado J, Sherkat N, Rothstein JD, Gage FH. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science. 2003;301:839-842.
46. Dobrowolny G, Giacinti C, Pelosi L, et al. Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol. 2005;168:193-199.
47. Adams GR, Haddad F, Baldwin KM. Time course of changes in markers of myogenesis in overloaded rat skeletal muscles. J Appl Physiol. 1999;87:1705-1712.
48. Schultz JD, Schlinger BA. Widespread accumulation of [H-3]testosterone in the spinal cord of a wild bird with an elaborate courtship display. Proc Natl Acad Sci USA. 1999;96:10428-10432.
49. Barske J, Schlinger BA, Wikelski M, Fusani L. Female choice for male motor skills. Proc R Soc Lond Ser B Biol Sci. 2011;278:3523-3528.
50. de Kort SR, Eldermire ERB, Valderrama S, Botero CA, Vehrencamp SL. Trill consistency is an age-related assessment signal in banded wrens. Proc R Soc B Biol Sci. 2009;276:2315-2321.
51. Sockman KW. Annual variation in vocal performance and its relationship with bill morphology in Lincoln's sparrows, Melospiza lincolnii. Anim Behav. 2009;77:663-671.
52. Behr O, von Helversen O. Bat serenades - complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol. 2004;56:106-115.
53. Pasch B, George AS, Hamlin HJ, Guillette LJ, Phelps SM. Androgens modulate song effort and aggression in neotropical singing mice. Horm Behav. 2011;59:90-97.
54. Podos J. A performance constraint on the evolution of trilled vocalizations in a songbird family (Passeriformes: Emberizdae). Evolution. 1997;51:537-551.
55. Pasch B, George AS, Campbell P, Phelps SM. Androgen-dependent male vocal performance influences female preference in neotropical singing mice. Anim Behav. 2011;82:177-183.
56. Illes AE, Hall ML, Vehrencamp SL. Vocal performance influences male receiver response in the banded wren. Proc R Soc B Biol Sci. 2006;273:1907-1912.
57. Dial KP. Activity patterns of the wing muscles of the pigeon (Columbia livia) during different modes of flight. J Exp Zool. 1992; 262:357-373.