In mid- to high-latitude songbirds, seasonal reproduction is stimulated by increasing day length accompanied by elevated plasma sex steroid levels, increased singing, and growth of the song control nuclei (SCN). Plasticity of the SCN and song behavior are primarily mediated by testosterone (T) and its metabolites in most species studied thus far. However, the majority of bird species are tropical and have less pronounced seasonal reproductive cycles. We have previously documented that equatorial rufous-collared sparrows (Zonotrichia capensis) exhibit seasonal neuroplasticity in the SCN. Manipulating T in these birds, however, did not alter singing behavior. In the current study, we investigated whether T mediates plasticity of the SCN in a similar manner to temperate songbirds. In the first experiment, we treated captive male birds with T or blank implants during the nonbreeding season. In a second experiment, we treated captive male birds with either blank implants, T-filled implants, T with flutamide (FLU; an androgen receptor antagonist) or T with FLU and 1,4,6-androstatriene-3,17-dione (ATD; an estrogen synthesis inhibitor) during the breeding season. In both experiments, the volumes of the brain areas high vocal center (HVC), Area X, and robust nucleus of the arcopallium (RA) were measured along with singing behavior. In summary, T stimulated growth of HVC and RA, and the combined effect of FLU and ATD reversed this effect in HVC. Area X was not affected by T treatment in either experiment. Neither T-treated birds nor controls sang in captivity during either experiment. Together, these data indicate that T mediates seasonal changes in the HVC and RA of both tropical and higher- latitude bird species even if the environmental signals differ. However, unlike most higher-latitude songbirds, we found no evidence that motivation to sing or growth of Area X are stimulated by T under captive conditions.

1.
Addis E, Busch DS, Clark AD, Wingfield JC (2010): Seasonal and social modulation of testosterone in Costa Rican rufous-collared sparrows (Zonotrichia capensis costaricensis). Gen Comp Endocrinol 166:581-589.
[PubMed]
2.
Alvarez-Borda B, Nottebohm F (2002): Gonads and singing play separate, additive roles in new neuron recruitment in adult Canary brain. J Neurosci 22:8684-8690.
[PubMed]
3.
Alward BA, Balthazart J, Ball GF (2013): Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc Natl Acad Sci USA 110:19573-19578.
[PubMed]
4.
Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters L V, Balthazart J (2004): Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann NY Acad Sci 1016:586-610.
[PubMed]
5.
Bentley GE, Van't Hof TJ, Ball GF (1999): Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc Natl Acad Sci USA 96:4674-4679.
[PubMed]
6.
Bernard DJ, Bentley GE, Balthazart J, Turek FW, Ball GF (1999): Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology 140:4633-4643.
[PubMed]
7.
Boseret G, Carere C, Ball GF, Balthazart J (2006): Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J Neurobiol 66:1044-1060.
[PubMed]
8.
Bradshaw WE, Holzapfel CM (2007): Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1-25.
9.
Brenowitz E (2008): Plasticity of the song control system in adult birds; in Zeigler HP, Marler P (eds): Neuroscience of Birdsong, Cambridge, Cambridge University Press, pp 330-347.
10.
Brenowitz EA, Baptista LF, Lent K, Wingfield JC (1998): Seasonal plasticity of the song control system in wild Nuttall's white-crowned sparrows. J Neurobiol 34:69-82.
[PubMed]
11.
Brenowitz EA, Lent K, Rubel EW (2007): Auditory feedback and song production do not regulate seasonal growth of song control circuits in adult white-crowned sparrows. J Neurosci 27:6810-6814.
[PubMed]
12.
Brenowitz EA, Zeigler HP, Marler P (2004): Plasticity of the adult avian song control system. Ann NY Acad Sci 1016:560-585.
[PubMed]
13.
Brown NL, Follett BK (1977): Effects of androgens on the testes of intact and hypophysectomized Japanese quail. Gen Comp Endocrinol 33:267-277.
[PubMed]
14.
Canoine V, Gwinner E (2002): Seasonal differences in the hormonal control of territorial aggression in free-living European stonechats. Horm Behav 41:1-8.
[PubMed]
15.
Cassone VM, Bartell PA, Earnest BJ, Kumar V (2008): Duration of melatonin regulates seasonal changes in song control nuclei of the house sparrow, Passer domesticus: independence from gonads and circadian entrainment. J Biol Rhythms 23:49-58.
[PubMed]
16.
Chandolia RK, Weinbauer GF, Simoni M, Behre HM, Nieschlag E (1991): Comparative effects of chronic administration of the non-steroidal antiandrogens flutamide and Casodex on the reproductive system of the adult male rat. Eur J Endocrinol 125:547-555.
[PubMed]
17.
Chesser R, Banks R, Barker F, Cicero C (2010): Fifty-first supplement to the American Ornithologists' Union check-list of North American birds. Auk 127:726-744.
18.
Cyr NE, Romero LM (2009): Identifying hormonal habituation in field studies of stress. Gen Comp Endocrinol 161:295-303.
[PubMed]
19.
DaCosta JM, Spellman GM, Escalante P, Klicka J (2009): A molecular systematic revision of two historically problematic songbird clades: Aimophila and Pipilo. J Avian Biol 40:206-216.
20.
Danner JE, Danner RM, Bonier F, Martin PR, Small TW, Moore IT (2011): Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence. Am Nat 178:53-63.
[PubMed]
21.
Dawson A (2003): Photoperiodic control of the annual cycle in birds and comparison with mammals. Ardea 90:355-367.
22.
Dawson A (2008): Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos Trans R Soc Lond B Biol Sci 363:1621-1633.
[PubMed]
23.
Desjardins C, Turek FW (1977): Effects of testosterone on spermatogenesis and luteinizing hormone release in Japanese quail. Gen Comp Endocrinol 33:293-303.
[PubMed]
24.
Deviche P, Hurley LL, Fokidis HB (2010): Avian testicular structure, function, and regulation; in Norris DO, Lopez KH (eds): Hormones and Reproduction of Vertebrates. New York, Academic Press, vol 1, pp 27-70.
25.
Deviche P, Martin RK, Small TW, Sharp PJ (2006): Testosterone induces testicular development but reduces GnRH-I fiber density in the brain of the house finch, Carpodacus mexicanus. Gen Comp Endocrinol 147:167-174.
[PubMed]
26.
Dickens MJ, Earle KA, Romero LM (2009): Initial transference of wild birds to captivity alters stress physiology. Gen Comp Endocrinol 160:76-83.
[PubMed]
27.
Dloniak SM, Deviche P (2001): Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis). Horm Behav 39:95-105.
[PubMed]
28.
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 166:66-71.
[PubMed]
29.
Fuchs E, Flügge G (2014): Adult neuroplasticity: more than 40 years of research. Neural Plast 2014;2014:541870.
[PubMed]
30.
Fusani L, Van't Hof T, Hutchison JB, Gahr M (2000): Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol 43:254-268.
[PubMed]
31.
Fusani L (2008): Endocrinology in field studies: problems and solutions for the experimental design. Gen Comp Endocrinol 157:249-253.
[PubMed]
32.
Gahr M (2001): Distribution of sex steroid hormone receptors in the avian brain: functional implications for neural sex differences and sexual behaviors. Microsc Res Tech 55:1-11.
[PubMed]
33.
Gahr M, Metzdorf R (1997): Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull 44:509-517.
[PubMed]
34.
González-Gómez PL, Merrill L, Ellis VA, Venegas C, Pantoja JI, Vasquez RA, Wingfield JC (2013): Breaking down seasonality: androgen modulation and stress response in a highly stable environment. Gen Comp Endocrinol 191:1-12.
[PubMed]
35.
Goymann W (2009): Social modulation of androgens in male birds. Gen Comp Endocrinol 163:149-157.
[PubMed]
36.
Hamner WM (1968): Photorefractory period of the house finch. Ecology 49:211-227.
37.
Hau M, Gill SA, Goymann W (2008): Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds. Gen Comp Endocrinol 157:241-248.
[PubMed]
38.
Hausberger M, Henry L, Richard MA (2010): Testosterone-induced singing in female European starlings (Sturnus vulgaris). Ethology 99:193-208.
39.
Kern MD, King JR (1972): Testosterone-induced singing in female white-crowned sparrows. Condor 74:204-209.
40.
Kim YH, Perlman WR, Arnold AP (2004): Expression of androgen receptor mRNA in zebra finch song system: developmental regulation by estrogen. J Comp Neurol 469:535-547.
[PubMed]
41.
Kumar V, Kumar BS (1990): Effect of testosterone on testes, body weight and plumage regeneration in photorefractory male redheaded bunting Emberiza bruniceps. Indian J Exp Biol 28:417-420.
[PubMed]
42.
Lahaye SEP, Eens M, Darras VM, Pinxten R (2012): Testosterone stimulates the expression of male-typical socio-sexual and song behaviors in female budgerigars (Melopsittacus undulatus): an experimental study. Gen Comp Endocrinol 178:82-88.
[PubMed]
43.
Leonard SLL (1939): Induction of singing in female canaries by injections of male hormone. Exp Biol Med 41:229-230.
44.
Lynn SE (2008): Behavioral insensitivity to testosterone: why and how does testosterone alter paternal and aggressive behavior in some avian species but not others? Gen Comp Endocrinol 157:233-240.
[PubMed]
45.
Lynn SE, Prince LE, Schook DM, Moore IT (2009): Supplementary testosterone inhibits paternal care in a tropically breeding sparrow, Zonotrichia capensis. Physiol Biochem Zool 82:699-708.
[PubMed]
46.
Madison FN, Rouse ML, Balthazart J, Ball GF (2014): Reversing song behavior phenotype: testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen Comp Endocrinol 215:61-75.
[PubMed]
47.
Mahler C, Verhelst J, Denis L (1998): Clinical pharmacokinetics of the antiandrogens and their efficacy in prostate cancer. Clin Pharmacokinet 34:405-417.
[PubMed]
48.
Mason GJ (2010): Species differences in responses to captivity: stress, welfare and the comparative method. Trends Ecol Evol 25:713-721.
[PubMed]
49.
Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ (2007): Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045-12057.
[PubMed]
50.
Meitzen J, Thompson CK, Choi H, Perkel DJ, Brenowitz EA (2009): Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition. Horm Behav 55:217-227.
[PubMed]
51.
Moore IT, Bentley GE, Wotus C, Wingfield JC (2006): Photoperiod-independent changes in immunoreactive brain gonadotropin-releasing hormone (GnRH) in a free-living, tropical bird. Brain Behav Evol 68:37-44.
[PubMed]
52.
Moore IT, Bonier F, Wingfield J (2005): Reproductive asynchrony and population divergence between two tropical bird populations. Behav Ecol 16:755-762.
53.
Moore IT, Perfito N, Wada H, Sperry TS, Wingfield JC (2002): Latitudinal variation in plasma testosterone levels in birds of the genus Zonotrichia. Gen Comp Endocrinol 129:13-19.
[PubMed]
54.
Moore IT, Wada H, Perfito N, Busch DS, Hahn TP, Wingfield JC (2004b): Territoriality and testosterone in an equatorial population of rufous-collared sparrows, Zonotrichia capensis. Anim Behav 67:411-420.
55.
Moore IT, Walker BG, Wingfield JC (2004a): The effects of combined aromatase inhibitor and anti-androgen on male territorial aggression in a tropical population of rufous-collared sparrows, Zonotrichia capensis. Gen Comp Endocrinol 135:223-229.
[PubMed]
56.
Moore IT, Wingfield JC (2002): Reproductive cycles in equatorial populations of rufous-collared sparrows, Zonotrichia capensis. Integr Comp Biol 42:1281.
57.
Moore IT, Wingfield JC, Brenowitz EA (2004c): Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J Neurosci 24:10182-10185.
[PubMed]
58.
Mougeot F, Redpath S, Piertney S, Hudson P (2005): Separating behavioral and physiological mechanisms in testosterone mediated trade-offs. Am Nat 166:158-168.
[PubMed]
59.
Newman AEM, MacDougall-Shackleton SA, An YS, Kriengwatana B, Soma KK (2010): Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system. J Comp Neurol 518:3662-3678.
[PubMed]
60.
Ohsako S, Kubota K, Kurosawa S, Takeda K, Qing W, Ishimura R, Tohyama C (2003): Alterations of gene expression in adult male rat testis and pituitary shortly after subacute administration of the antiandrogen flutamide. J Reprod Dev 49:275-290.
[PubMed]
61.
Quispe R, Trappschuh M, Gahr M, Goymann W (2015): Towards more physiological manipulations of hormones in field studies: comparing the release dynamics of three kinds of testosterone implants, silastic tubing, time-release pellets and beeswax. Gen Comp Endocrinol 212:100-105.
[PubMed]
62.
Robertson BD, Hasstedt MR, Vandermeer CL, MacDougall-Shackleton SA (2014): Sex steroid-independent effects of photostimulation on the song-control system of white-throated sparrows (Zonotrichia albicollis). Gen Comp Endocrinol 204C:166-172.
[PubMed]
63.
Sartor JJ, Ball GF (2005a): Activity-dependent regulation of seasonal neuroplasticity in the song system in songbirds; in Dawson A, Sharp PJ (eds): Functional Avian Endocrinology. New Delhi, Narosa Publishing House, pp 355-360.
64.
Sartor JJ, Ball GF (2005b): Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci 119:233-244.
[PubMed]
65.
Small TW, Sharp PJ, Bentley GE, Deviche P (2008b): Relative photorefractoriness, prolactin, and reproductive regression in a flexibly breeding sonoran desert passerine, the rufous-winged sparrow, Aimophila carpalis. J Biol Rhythms 23:69-80.
[PubMed]
66.
Small TW, Sharp PJ, Bentley GE, Millar RP, Tsutsui K, Mura E, Deviche P (2008a): Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living Sonoran Desert bird, the rufous-winged sparrow (Aimophila carpalis). Brain Behav Evol 71:127-142.
[PubMed]
67.
Small TW, Sharp PJ, Deviche P (2007): Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the rufous-winged sparrow, Aimophila carpalis. Horm Behav 51:483-495.
[PubMed]
68.
Smith GT, Brenowitz EA, Wingfield JC (1997): Seasonal changes in the size of the avian song control nucleus HVC defined by multiple histological markers. J Comp Neurol 381:253-261.
[PubMed]
69.
Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995): Seasonal changes in song nuclei and song behavior in Gambel's White-crowned Sparrows. J Neurobiol 28:114-125.
[PubMed]
70.
Soma KK, Hartman VN, Wingfield JC, Brenowitz EA (1999a): Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J Comp Neurol 409:224-236.
[PubMed]
71.
Soma KK, Sullivan K, Wingfield J (1999b): Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen Comp Endocrinol 115:442-453.
[PubMed]
72.
Stevenson TJ, Small TW, Ball GF, Moore IT (2012): Variation in the gonadotrophin-releasing hormone-1 and the song control system in the tropical breeding rufous-collared sparrow (Zonotrichia capensis) is dependent on sex and reproductive state. Gen Comp Endocrinol 178:1-7.
[PubMed]
73.
Strand CR, Ross MS, Weiss SL, Deviche P (2008): Testosterone and social context affect singing behavior but not song control region volumes in adult male songbirds in the fall. Behav Processes 78:29-37.
[PubMed]
74.
Strand CR, Small TW, Deviche P (2007): Plasticity of the rufous-winged sparrow, Aimophila carpalis, song control regions during the monsoon-associated summer breeding period. Horm Behav 52:401-408.
[PubMed]
75.
Stutchbury BJM, Morton ES (2001): Behavioral Ecology of Tropical Birds. San Diego, Academic Press.
76.
Thompson CK, Brenowitz EA (2005): Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J Comp Neurol 481:276-283.
[PubMed]
77.
Tokarz R (1987): Effects of the antiandrogens cyproterone acetate and flutamide on male reproductive behavior in a lizard (Anolis sagrei). Horm Behav 21:1-16.
[PubMed]
78.
Tramontin AD, Brenowitz EA (2000): Seasonal plasticity in the adult brain. Trends Neurosci 23:251-258.
[PubMed]
79.
Tramontin AD, Hartman VN, Brenowitz EA (2000): Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J Neurosci 20:854-861.
[PubMed]
80.
Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998): Seasonal plasticity and sexual dimorphism in the avian song control system: stereological measurement of neuron density and number. J Comp Neurol 396:186-192.
[PubMed]
81.
Tramontin AD, Wingfield JC, Brenowitz EA (1999): Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J Neurosci 19:476-483.
[PubMed]
82.
Turek FW, Desjardins C, Menaker M (1976): Anti-gonadal and pro-gonadal effects of testosterone in male House Sparrows. Gen Comp Endocrinol 28:395-402.
[PubMed]
83.
Turek FW, Wolfson A, Desjardins C (1980): Testosterone treatment blocks the termination of the gonadal photorefractory condition in white-throated sparrows maintained on short days. Gen Comp Endocrinol 41:365-371.
[PubMed]
84.
Vagell ME, McGinnis MY (1998): The role of gonadal steroid receptor activation in the restoration of sociosexual behavior in adult male rats. Horm Behav 33:163-179.
[PubMed]
85.
Viguier-Martinez MC, Hochereau-de Reviers MT, Perreau C (1985): Effects of flutamide or of supplementation with testosterone in prepubertal male rats prenatally treated with busulfan. Eur J Endocrinol 109:550-557.
86.
Wacker DW, Wingfield JC, Davis JE, Meddle SL (2010): Seasonal changes in aromatase and androgen receptor, but not estrogen receptor mRNA expression in the brain of the free-living male song sparrow, Melospiza melodia morphna. J Comp Neurol 518:3819-3835.
[PubMed]
87.
Wada K, Hayase S, Imai R, Mori C, Kobayashi M, Liu WC, Takahasi M, Okanoya K (2013): Differential androgen receptor expression and DNA methylation state in striatum song nucleus Area X between wild and domesticated songbird strains. Eur J Neurosci 38:2600-2610.
[PubMed]
88.
Wiley C (2003): Testosterone is correlated with courtship but not aggression in the tropical buff-banded rail, Gallirallus philippensis. Horm Behav 43:554-560.
[PubMed]
89.
Williams TD (2008): Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean'. Philos Trans R Soc Lond B Biol Sci 363:1687-1698.
[PubMed]
90.
Wingfield JC, Meddle SL, Moore IT, Busch S, Wacker DW, Lynn S, Clark A, Vasquez RA, Addis E (2007): Endocrine responsiveness to social challenges in northern and southern hemisphere populations of Zonotrichia. J Ornithol 148:435-441.
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