Neurogenomic mechanisms of aggression in songbirds

Advances in Genetics

Volumn 75, Issue , 2011, Pages 83-119

  Maney, Donna L ^a   Goodson, James L ^b  

^a EMORY UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Challenge hypothesis; Dominance; Dopamine; Field endocrinology; Immediate early genes; Social behavior network; Territoriality; Testosterone; Vasotocin; White throated sparrow

Indexed keywords

EID: 81055127032     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-380858-5.00002-2     Document Type: Chapter

References (190)

1. Adkins-Regan E. Hormones and Animal Social Behavior 2005, Princeton University Press, Princeton.
2. Allee W.C. Analytical studies of group behavior in birds. Wilson Bull. 1936, 48:145-151.
3. Allee W.C. Group organization among vertebrates. Science 1942, 95:289-293.
4. Allee W.C., Collias N.E., Lutherman C.Z. Modification of the social order in flocks of hens by the injection of testosterone propionate. Physiol. Zool. 1939, 12:412-440.
5. Arcese P., Sogge M.K., Marr A.B., Patten M.A. Song Sparrow (Melospiza melodia). The Birds of North America Online 2002, Cornell Lab of Ornithology, Ithaca. 10.2173/bna.704. A. Poole (Ed.).
6. Archawaranon M., Wiley R.H. Control of aggression and dominance in white-throated sparrows by testosterone and its metabolites. Horm. Behav. 1988, 22:497-517.
7. Archawaranon M., Dove L., Wiley R.H. Social inertia and hormonal control of aggression and dominance in white-throated sparrows. Behaviour 1991, 118:42-65.
8. Archer J. Testosterone and human aggression: An evaluation of the challenge hypothesis. Neurosci. Biobehav. Rev. 2006, 30:319-345.
9. Aromaki A.S., Lindman R.E., Eriksson C.J.P. Testosterone, aggressiveness, and antisocial personality. Aggress. Behav. 1999, 25:113-123.
10. Aste N., Viglietti-Panzica C., Balthazart J., Panzica G.C. Testosterone modulation of peptidergic pathways in the septo-preoptic region of male Japanese quail. Poult. Avian Biol. Rev. 1997, 8:77-93.
11. Ball G.F., Balthazart J. Ethological concepts revisited: Immediate early gene induction in response to sexual stimuli in birds. Brain Behav. Evol. 2001, 57:252-270.
12. Baptista L.F., DeWolfe B.B., Avery-Beausoleil L. Testosterone, aggression, and dominance in Gambel's white-crowned sparrows. Wilson Bull. 1987, 99:86-91.
13. Baptista L.F., Trail P.W., DeWolfe B.B., Morton M.L. Singing and its functions in female white-crowned sparrows. Anim. Behav. 1993, 46:511-524.
14. Berg S., Wynne-Edwards K.E. Changes in testosterone, cortisol, and estradiol levels in men becoming fathers. Mayo Clin. Proc. 2001, 76:582-592.
15. Bernhardt P.C., Dabbs J.M., Fielden J.A., Lutter C.D. Testosterone changes during vicarious experiences of winning and losing among fans at sporting events. Physiol. Behav. 1998, 65:59-62.
16. Bharati I.S., Goodson J.L. Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 2006, 143:661-670.
17. Blanchard D.C., Blanchard R.J. What can animal aggression research tell us about human aggression?. Horm. Behav. 2003, 44:171-177.
18. Blanchard R.J., Blanchard D.C. Some suggestions for revitalizing aggression research. Novartis Found. Symp. 2005, 268:4-12.
19. Book A.S., Starzyk K.B., Quinsey V.L. The relationship between testosterone and aggression: A meta-analysis. Aggr. Viol. Behav. 2001, 6:579-599.
20. Booth A., Shelley G., Mazur A., Tharp G., Kittok R. Testosterone, and winning and losing in human competition. Horm. Behav. 1989, 23:556-571.
21. Buchanan K.L., Evans M.R., Roberts M.L., Rowe L., Goldsmith A.R. Does testosterone determine dominance in the house sparrow Passer domesticus? An experimental test. J. Avian Biol. 2010, 41:445-451.
22. Bullock T.H. Comparative neuroscience holds promise for quiet revolutions. Science 1984, 225:473-478.
23. Carey M., Burhans D.E., Nelson D.A. Field Sparrow (Spizella pusilla). The Birds of North America Online 2008, Cornell Lab of Ornithology, Ithaca. 10.2173/bna.103. A. Poole (Ed.).
24. Chase I.D. Dynamics of hierarchy formation: The sequential development of dominance relationships. Behaviour 1982, 80:218-240.
25. Chilton G., Baker M.C., Barrentine C.D., Cunningham M.A. White-CrownedSparrow (Zonotrichia leucophrys). The Birds of North America Online 1995, Cornell Lab of Ornithology, Ithaca. 10.2173/bna.183. A. Poole (Ed.).
26. Collins C.E., Houtman A.M. Tan and white color morphs of white-throated sparrows differ in their non-song vocal responses to territorial intrusion. Condor 1999, 101:842-845.
27. Crews D., Lou W., Fleming A., Ogawa S. From gene networks underlying sex determination and gonadal differentiation to the development of neural networks regulating sociosexual behavior. Brain Res. 2006, 1126:109-121.
28. Crook J.H., Butterfield P.A. Effects of testosterone propionate and luteinizing hormone on agonistic and nest building behavior of Quelea quelea. Anim. Behav. 1968, 16:370-384.
29. Dabbs J.M., Morris R. Testosterone, social class, and antisocial behavior in a sample of 4,462 men. Psychol. Sci. 1990, 1:209-211.
30. Dabbs J.M., Strong R., Milun R. Exploring the mind of testosterone: A bleeper study. J. Res. Pers. 1997, 31:577-587.
31. Daitzman R., Zuckerman M. Disinhibitory sensation seeking, personality and gonadal hormones. Pers. Individ. Diff. 1980, 1:103-110.
32. Davis J.K., Lowman J.J., Thomas P.J., ten Hallers B.F.H., Koriabine M., Huynh L.Y., Maney D.L., de Jong P.J., Martin C.L., Thomas J.W. Evolution of a bitter taste receptor gene cluster in a New World sparrow. Genome Biol. Evol. 2010, 2:358-370. NISC Comparative Sequencing Program.
33. Davis J.K., Mittel L.X., Lowman J.J., Thomas P.J., Maney D.L., Martin C.L., Thomas J.W. Haplotype-based genetic sequencing of a chromosomal polymorphism in the white-throated sparrow (Zonotrichia albicollis). J. Heredity 2011, NISC Comparative Sequencing Program, (accepted with minor revision).
34. Dawson A., Kin V.M., Bentley G.E., Ball G.F. Photoperiodic control of seasonality in birds. J. Biol. Rhythms 2001, 16:365-380.
35. Dearborn D.C., Wiley R.H. Prior residence has a gradual influence on the dominance in captive white-throated sparrows. Anim. Behav. 1993, 46:39-46.
36. Dufty A.M., Wingfield J.C. The influence of social cues on the reproductive endocrinology of male brown-headed cowbirds: Field and laboratory studies. Horm. Behav. 1986, 20:222-234.
37. Edens F.W. Agonistic behavior and neurochemistry in grouped Japanese quail. Comp. Biochem. Physiol. A Comp. Physiol. 1987, 86:473-479.
38. Elekonich M.M. Female song sparrow, Melospiza melodia, response to simulated conspecific and heterospecific intrusion across three seasons. Anim. Behav. 2000, 59:551-557.
39. Falls J.B. Functions of territorial song in the white-throated sparrow. Bird Vocalizations 1969, 207-232. Cambridge University Press, Cambridge. R.A. Hinde (Ed.).
40. Falls J.B. Does song deter territorial intrusion in white-throated sparrows (Zonotrichia albicollis)?. Can. J. Zool. 1988, 66:206-211.
41. Falls J.B., Kopachena J.G. White-Throated Sparrow (Zonotrichia albicollis), The Birds of North America Online 2010, Cornell Lab of Ornithology, Ithaca. 10.2173/bna.128. A. Poole (Ed.).
42. Ficken R.W., Ficken M.S., Hailman J.P. Differential aggression in genetically different morphs of the white-throated sparrow (Zonotrichia albicollis). Z. Tierpsychol. 1978, 46:43-57.
43. Finch C.E., Rose M.R. Hormones and the physiological architecture of life history evolution. Quart. Rev. Biol. 1995, 70:1-52.
44. Fleming A.S., Corter C., Stallings J., Steiner M. Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Horm. Behav. 2002, 42:399-413.
45. Gammie S.C. Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav. Cogn. Neurosci. Rev. 2005, 4:119-135.
46. Goldman P. Song recognition by field sparrows. Auk 1973, 90:103-113.
47. Goodson J.L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 1998, 34:67-77.
48. Goodson J.L. Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol. 1998, 111:233-244.
49. Goodson J.L. The vertebrate social behavior network: Evolutionary themes and variations. Horm. Behav. 2005, 48:11-22.
50. Goodson J.L., Bass A.H. Vocal-acoustic circuitry and descending vocal pathways in teleost fish: Convergence with terrestrial vertebrates reveals conserved traits. J. Comp. Neurol. 2002, 448:298-322.
51. Goodson J.L., Evans A.K. Neural responses to territorial challenge and nonsocial stress in male song sparrows: Segregation, integration, and modulation by a vasopressin V1 antagonist. Horm. Behav. 2004, 46:371-381.
52. Goodson J.L., Kabelik D. Dynamic limbic networks and social diversity in vertebrates: From neural context to neuromodulatory patterning. Front. Neuroendocrinol. 2009, 30:429-441.
53. Goodson J.L., Wang Y. Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species. Proc. Natl. Acad. Sci. USA 2006, 103:17013-17017.
54. Goodson J.L., Eibach R., Sakata J., Adkins-Regan E. Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla). Behav. Brain Res. 1999, 98:167-180.
55. Goodson J.L., Evans A.K., Lindberg L. Chemoarchitectonic subdivisions of the songbird septum and a comparative overview of septum chemical anatomy in jawed vertebrates. J. Comp. Neurol. 2004, 473:293-314.
56. Goodson J.L., Lindberg L., Johnson P. Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches. Horm. Behav. 2004, 45:136-143.
57. Goodson J.L., Saldanha C.J., Hahn T.P., Soma K.K. Recent advances in behavioral neuroendocrinology: Insights from studies on birds. Horm. Behav. 2005, 48:461-473.
58. Goodson J.L., Evans A.K., Lindberg L., Allen C.D. Neuro-evolutionary patterning of sociality. Proc. R. Soc. Lond. B 2005, 272:227-235.
59. Goodson J.L., Evans A.K., Soma K.K. Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. Neuroreport 2005, 16:1719-1723.
60. Goodson J.L., Kabelik D., Kelly A.M., Rinaldi J., Klatt J.D. Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proc. Natl. Acad. Sci. USA 2009, 106:8737-8742.
61. Goodson J.L., Kabelik D., Schrock S.E. Dynamic neuromodulation of aggression by vasotocin: Influence of social context and social phenotype in territorial songbirds. Biol. Lett. 2009, 5:554-556.
62. Goodson J.L., Rinaldi J., Kelly A.M. Vasotocin neurons in the bed nucleus of the stria terminalis preferentially process social information and exhibit properties that dichotomize courting and non-courting phenotypes. Horm. Behav. 2009, 55:197-202.
63. Gray P.B. Marriage, parenting, and testosterone variation among Kenyan Swahili men. Am. J. Phys. Anthropol. 2003, 122:279-286.
64. Gray P.B., Kahlenberg S.M., Barret E.S., Lipson S.F., Ellison P.T. Marriage and fatherhood are associated with low testosterone in males. Evol. Hum. Behav. 2002, 23:193-201.
65. Guhl A.M. Social inertia and social stability in chickens. Anim. Behav. 1968, 16:219-232.
66. Hamilton W.D. Geometry for the selfish herd. J. Theoret. Biol. 1971, 31:295-311.
67. Harrington B.A. Aggression in winter resident and spring migrant white-throated sparrows in Massachusetts. Bird Banding 1973, 44:314-315.
68. Hau M. Regulation of male traits by testosterone: Implications for the evolution of vertebrate life histories. Bioessays 2007, 292:133-144.
69. Hegner R.E., Wingfield J.C. Behavioral and endocrine correlates of multiple brooding in the semi-colonial house sparrow Passer domesticus I. Males. Horm. Behav. 1986, 20:294-312.
70. Hegner R.E., Wingfield J.C. Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 1987, 104:462-469.
71. Heimovics S.A., Cornil C.A., Ball G.F., Riters L.V. D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings. Neuroscience 2009, 159:962-973.
72. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 1998, 28:370-490.
73. Ho J.M., Murray J.H., Demas G.E., Goodson J.L. Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice. Horm. Behav. 2010, 58:368-377.
74. Hoke K.L., Ryan M.J., Wilczynski W. Social cues shift functional connectivity in the hypothalamus. Proc. Natl. Acad. Sci. USA 2005, 102:10712-10717.
75. Huynh L.Y., Maney D.L., Thomas J.W. Chromosome-wide linkage disequilibrium caused by an inversion polymorphism in the white-throated sparrow. Heredity 2010, (in press).
76. Huynh L.Y., Maney D.L., Thomas J.W. Contrasting population genetic patterns within the white-throated sparrow genome (Zonotrichia albicollis). BMC Genomics 2010, 11:96.
77. Insel T.R., Fernald R.D. How the brain processes social information: Searching for the social brain. Annu. Rev. Neurosci. 2004, 27:697-722.
78. Julian T., McHenry P.C. Relationship of testosterone to men's family functioning at mid-life: A research note. Aggress. Behav. 1989, 15:281-289.
79. Kabelik D., Klatt J.D., Kingsbury M.A., Goodson J.L. Endogenous vasotocin exerts context-dependent behavioral effects in a semi-naturalistic colony environment. Horm. Behav. 2009, 56:101-107.
80. Kabelik D., Kelly A.M., Goodson J.L. Dopaminergic regulation of mate competition aggression and aromatase-Fos colocalization in vasotocin neurons. Neuropharmacology 2010, 58:117-125.
81. Ketterson E.D., Nolan V. Hormones and life histories: An integrative approach. Am. Nat. 1992, 140:S33-S62.
82. Ketterson E.D., Nolan V. Male parental behavior in birds. Annu. Rev. Ecol. Syst. 1994, 25:601-628.
83. Keys G.C., Rothstein S.I. Benefits and costs of dominance and subordinance in white-crowned sparrows and the paradox of status signalling. Anim. Behav. 1991, 42:899-912.
84. Kingsbury M.A., Kelly A.M., Schrock S.E., Goodson J.L. Mammal-like organization of the avian midbrain central gray and a reappraisal of the intercollicular nucleus. PLoS One 2011.
85. Knapton R.W., Falls J.B. Differences in parental contribution among pair types in the polymorphic white-throated sparrow. Can. J. Zool. 1983, 61:1288-1292.
86. Kollack-Walker S., Watson S.J., Akil H. Social stress in hamsters: Defeat activates specific neurocircuits within the brain. J. Neurosci. 1997, 17:8842-8855.
87. Konishi M., Emlen S.T., Ricklefs R.E., Wingfield J.C. Contributions of bird studies to biology. Science 1989, 246:465-472.
88. Kopachena J.G., Falls J.B. Aggressive performance as a behavioral correlate of plumage polymorphism in the white-throated sparrow (Zonotrichia albicollis). Behaviour 1993, 124:249-266.
89. Kopachena J.G., Falls J.B. Re-evaluation of morph-specific variations in parental behavior of the white-throated sparrow. Wilson Bull. 1993, 105:48-59.
90. Kotegawa T., Abe T., Tsutsui K. Inhibitory role of opioid peptides in the regulation of aggressive and sexual behaviors in male Japanese quails. J. Exp. Zool. 1997, 277:146-154.
91. Krebs J.R. Territory and breeding density in the great tit, Parus major. Ecology 1971, 52:2-22.
92. Krebs J. Bird song and territorial defence. New Sci. 1976, 70:534-536.
93. Kroodsma D.E. The effect of large song repertoires on neighbor "recognition" in male song sparrows. Condor 1976, 78:97-99.
94. Kroodsma D.E., Bereson R.C., Byers B.E., Minear E. Use of song types by the chestnut-sided warbler: Evidence for both intra- and inter-sexual functions. Can. J. Zool. 1989, 67:447-456.
95. Lein M.R. Song variation in a population of chestnut-sided warblers (Dendroica pensylvanica): Its nature and suggested significance. Can. J. Zool. 1978, 56:1266-1283.
96. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-226.
97. Lowther J.K. Polymorphism in the white-throated sparrow, Zonotrichia albicollis (Gmelin). Can. J. Zool. 1961, 39:281-292.
98. Lumia A.R. The relationships among testosterone, conditioned aggression, and dominance in male pigeons. Horm. Behav. 1972, 3:277-286.
99. Maney D.L. Endocrine and genomic architecture of life history trade-offs in an avian model of social behavior. Gen. Comp. Endocrinol. 2008, 157:275-282.
100. Maney D.L. Hormonal control of sexual behavior in female nonmammalian vertebrates. Encyclopedia of Animal Behavior 2010, Vol. 1:697-703. Elsevier, Oxford.
101. Maney D.L., Ball G.F. Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J. Neurobiol. 2003, 56:163-170.
102. Maney D.L., Goode C.T., Wingfield J.C. Intraventricular infusion of arginine vasotocin induces singing in a female songbird. J. Neuroendocrinol. 1997, 9:487-491.
103. Maney D.L., Erwin K.L., Goode C.T. Neuroendocrine correlates of behavioral polymorphism in white-throated sparrows. Horm. Behav. 2005, 48:196-206.
104. Maney D.L., Lange H.S., Raees M.Q., Sanford S.E. Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows. Horm. Behav. 2009, 55:113-120.
105. Mathewson S.F. Gonadotrophic hormones affect aggressive behavior in starlings. Science 1961, 134:1522-1523.
106. Maynard-Smith J. Parental investment: A prospective analysis. Anim. Behav. 1977, 25:1-9.
107. McGlothlin J.W., Ketterson E.D. Hormone-mediated suites as adaptations and evolutionary constraints. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007, 170:864-875.
108. McGlothlin J.W., Jawor J.M., Ketterson E.D. Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. Am. Nat. 2007, 170:864-875.
109. Mello C.V., Ribeiro S. ZENK protein regulation by song in the brain of songbirds. J. Comp. Neurol. 1998, 393:426-438.
110. Mello C.V., Vicario D.S., Clayton D.F. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. USA 1992, 89:6818-6822.
111. Miles D.B., Sinervo B., Hazard L.C., Svensson E.I., Costa D. Relating endocrinology, physiology and behaviour using species with alternative mating strategies. Funct. Ecol. 2007, 21:653-665.
112. Møller A.P. Variation in badge size in male house sparrows Passer domesticus: Evidence for status signalling. Anim. Behav. 1987, 35:1637-1644.
113. Moore M.C. Effect of female displays on the endocrine physiology and behavior of male white-crowned sparrows, Zonotrichia leucophrys. J. Zool. 1983, 199:137-148.
114. Moore M.C. Application of organization-activation theory to alternative male reproductive strategies: A review. Horm. Behav. 1991, 25:154-179.
115. Motta S.C., Goto M., Gouveia F.V., Baldo M.V.C., Canteras N.S., Swanson L.W. Dissecting the brain's fear system reveals the hypothalamus is critical for responding in subordinate conspecific intruders. Proc. Natl. Acad. Sci. 2009, 106:4870-4875.
116. Moyer K.E. Kinds of aggression and their physiological basis. Commun. Behav. Biol. 1968, 2(A):65-87.
117. Mukai M., Replogle K., Drnevich J., Wang G., Wacker D., Band M., Clayton D.F., Wingfield J.C. Seasonal differences of gene expression profiles in song sparrow (Melospiza melodia) hypothalamus in relation to territorial aggression. PLoS One 2009, 4:e8182.
118. Nelson D.A., Croner L.J. Song categories and their functions in the field sparrow (Spizella pusilla). Auk 1991, 108:42-52.
119. Newman S.W. The medial extended amygdala in male reproductive behavior: A node in the mammalian social behavior network. Ann. N.Y. Acad. Sci. 1999, 877:242-257.
120. Nice M.M. Studies in the Life History of the Song Sparrow. II. The Behaviour of the Song Sparrow and Other Passerines 1943, Dover, New York.
121. Nijhout F.H. Development and evolution of adaptive polyphenisms. Evol. Dev. 2003, 5:9-18.
122. Nolan V., Ketterson E.D., Cristol D.A., Rogers C.M., Clotfelter E.D., Titus R.C., Schoech S.J., Snajdr E. Dark-eyed Junco (Junco hyemalis). The Birds of North America Online 2002, Cornell Lab of Ornithology, Ithaca, doi:10.2173/bna.716. A. Poole (Ed.).
123. Panzica G.C., Aste N., Castagna C., Viglietti-Panzica C., Balthazart J. Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: Behavioral implications. Brain Res. Rev. 2001, 37:178-200.
124. Piper W.H., Wiley R.H. Correlates of dominance in wintering white-throated sparrows: Age, sex and location. Anim. Behav. 1989, 37:298-310.
125. Pradhan D.S., Newman A.E., Wacker D.W., Wingfield J.C., Schlinger B.A., Soma K.K. Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm. Behav. 2010, 57:381-389.
126. Ramenofsky M. Agonistic behavior and endogenous plasma hormones in male Japanese quail. Anim. Behav. 1984, 32:698-708.
127. Ramirez J.M., Salas C., Portavella M. Offense and defense after lateral septal lesions in Columba livia. Int. J. Neurosci. 1988, 41:241-250.
128. Remage-Healey L., Maidment N.T., Schlinger B.A. Forebrain steroid levels fluctuate rapidly during social interactions. Nat. Neurosci. 2008, 11:1327-1334.
129. Remage-Healey L., London S.E., Schlinger B.A. Birdsong and the neural production of steroids. J. Chem. Neuroanat. 2010, 39:72-81.
130. Rhen T., Crews D. Variation in reproductive behaviour within a sex: Neural systems and endocrine activation. J. Neuroendocrinol. 2002, 14:517-531.
131. Robinson G.E., Grozinger C.M., Whitfield C.W. Sociogenomics: Social life in molecular terms. Nat. Rev. Genet. 2005, 6:257-270.
132. Rohwer S. The social significance of avian winter plumage variability. Evolution 1975, 29:593-610.
133. Rohwer S., Rohwer F.C. Status signalling in Harris sparrows: Experimental deceptions achieved. Anim. Behav. 1978, 26:1012-1022.
134. Romanov M.N., Tuttle E.M., Houck M.L., Modi W.S., Chemnick L.G., Korody M.L., et al. The value of avian genomics to the conservation of wildlife. BMC Genomics 2009, 10:S10.
135. Sabine W.S. The winter society of the Oregon Junco: Intolerance, dominance, and the pecking order. Condor 1959, 61:110-135.
136. Schlinger B.A. Plasma androgens and aggressiveness in captive winter white-throated sparrows (Zonotrichia albicollis). Horm. Behav. 1987, 21:203-210.
137. Schneider K.C.J. Dominance, predation, and optimal foraging in white-throated sparrow flocks. Ecology 1984, 65:1820-1827.
138. Schoech S.J., Ketterson E.D., Nolan V., Sharp P.J., Buntin J.D. The effect of exogenous testosterone on parental behavior, plasma prolactin, and prolactin binding sites in the dark-eyed juncos. Horm. Behav. 1998, 34:1-10.
139. Schroeder M.B., Riters L.V. Pharmacological manipulations of dopamine and opioids have differential effects on sexually motivated song in male European starlings. Physiol. Behav. 2006, 88:575-584.
140. Schwabl H., Ramenofsky M., Schwabl-Benzinger I., Farner D.S., Wingfield J.C. Social status, circulating levels of hormones, and competition for food in winter flocks of the white-throated sparrow. Behaviour 1988, 107:107-121.
141. Selinger H.E., Bermant G. Hormonal control of aggressive behavior in Japanese quail (Coturnix coturnix japonica). Behavior 1967, 28:255-268.
142. Silverin B. Effects of long-acting testosterone treatment on free living pied flycatchers, Ficedula hypoleuca, during the breeding season. Anim. Behav. 1980, 28:906-912.
143. Sinervo B., Svensson E. Correlational selection and the evolution of genomic architecture. Heredity 2002, 89:329-338.
144. Soma K.K. Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol. 2006, 18:543-551.
145. Soma K.K., Wingfield J.C. Dehydroepiandrosterone in songbird plasma: Seasonal regulation and relationship to territorial aggression. Gen. Comp. Endocrinol. 2001, 123:144-155.
146. Soma K.K., Sullivan K., Wingfield J.C. Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen. Comp. Endocrinol. 1999, 115:442-453.
147. Soma K.K., Tramontin A.D., Wingfield J.C. Oestrogen regulates male aggression in the non-breeding season. Proc. R. Soc. Lond. B Biol. Sci. 2000, 267:1089-1096.
148. Soma K.K., Sullivan K.A., Tramontin A.D., Saldanha C.J., Schlinger B.A., Wingfield J.C. 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.
149. Soma K.K., Schlinger B.A., Wingfield J.C., Saldanha C.J. Brain aromatase, 5-alpha reductase, and 5-beta reductase change seasonally in wild male song sparrows: Relationship to aggressive and sexual behavior. J. Neurobiol. 2003, 56:209-221.
150. Soma K.K., Scotti M.A., Newman A.E., Charlier T.D., Demas G.E. Novel mechanisms for neuroendocrine regulation of aggression. Front. Neuroendocrinol. 2008, 29:476-489.
151. Spinney L.H., Bentley G.E., Hau M. Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis). Horm. Behav. 2006, 50:762-771.
152. Storey A.E., Walch C.J., Quinton R.L., Wynne-Edwards K.E. Hormonal correlates of paternal responsiveness in new and expectant fathers. Evol. Hum. Behav. 2000, 21:79-95.
153. Swett M.B., Breuner C.W. Plasma testosterone correlates with morph type across breeding substages in male white-throated sparrows. Physiol. Biochem. Zool. 2009, 82:572-579.
154. Thomas J.W., Cáceres M., Lowman J.J., Morehouse C.B., Short M.E., Baldwin E.L., Maney D.L., Martin C.L. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement that suppresses recombination. Genetics 2008, 179:1455-1468.
155. Thorneycroft H.B. A cytogenetic study of the white-throated sparrow, Zonotrichia albicollis. Evolution 1975, 29:611-621.
156. Tompkins G. Individuality and territoriality as displayed in winter by three passerine species. Condor 1933, 35:98-106.
157. Trainor B.C., Finy M.S., Nelson R.J. Paternal aggression in a biparental mouse: Parallels with maternal aggression. Horm. Behav. 2008, 53:200-207.
158. Trivers R.L. Parental investment and sexual selection. Sexual Selection and the Descent of Man 1972, 139-179. Aldine, Chicago. B. Campbell (Ed.).
159. Tuttle E.M. Mate choice and stable polymorphism in the white-throated sparrow 1993, State University of New York at Albany, Ph.D, Dissertation.
160. Tuttle E.M. Alternative reproductive strategies in the white-throated sparrow: Behavioral and genetic evidence. Behav. Ecol. 2003, 14:425-432.
161. Udry J.R. Biosocial models of adolescent problem behaviors. Social Biol. 1990, 37:1-10.
162. Veenema A.H., Bredewold R., Neumann I.D. Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: Link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 2007, 32:437-450.
163. Voorhuis T.A.M., Kiss J.Z., de Kloet E.R., de Wied D. Testosterone-sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res. 1988, 442:139-146.
164. Wacker D.W., Schlinger B.A., Wingfield J.C. Combined effects of DHEA and fadrozole on aggression and neural VIP immunoreactivity in the non-breeding male song sparrow. Horm Behav. 2008, 53:287-294.
165. Wacker D.W., Wingfield J.C., Davis J.E., Meddle S.L. 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. 2010, 518:3819-3835.
166. Walker B.G., Boersma P.D., Wingfield J.C. Field endocrinology and conservation biology. Integr. Comp. Biol. 2005, 45:12-18.
167. Warren W.C., Clayton D.F., Ellegren H., Arnold A.P., Hillier L.W., Künstner A., et al. The genome of a songbird. Nature 2010, 464:757-762.
168. Watt D.J. Plumage brightness index for white-throated sparrows. J. Field Ornithol. 1986, 57:105-113.
169. Watt D.J., Ralph C.J., Atkinson C.T. The role of plumage polymorphism in dominance relationships of the white-throated sparrow. Auk 1984, 101:110-120.
170. Wiley R.H., Piper W.H., Archawaranon M., Thompson E.W. Singing in relation to social dominance and testosterone in white-throated sparrows. Behaviour 1993, 127:175-190.
171. Wiley R.H., Steadman L., Chawick L., Wollerman L. Social inertia in white-throated sparrows results from recognition of opponents. Anim. Behav. 1999, 57:453-463.
172. Wingfield J.C. Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia I. Temporal organization of the breeding cycle. Gen. Comp. Endocrinol. 1984, 56:406-416.
173. Wingfield J.C. Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia II. Agonistic interactions as environmental information stimulating secretion of testosterone. Gen. Comp. Endocrinol. 1984, 56:417-424.
174. Wingfield J.C. Androgens and mating systems: Testosterone-induced polygyny in normally monogamous birds. Auk 1984, 101:665-671.
175. Wingfield J.C. Short-term changes in plasma levels of hormones during establishment and defense of a breeding territory in male song sparrows, Melospiza melodia. Horm. Behav. 1985, 19:174-187.
176. Wingfield J.C. Control of territorial aggression in a changing environment. Psychoneuroendocrinology 1994, 19:709-721.
177. Wingfield J.C. Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm. Behav. 1994, 28:1-15.
178. Wingfield J.C., Farner D.S. Avian endocrinology-Field investigations and methods. Condor 1976, 78:570-573.
179. Wingfield J.C., Farner D.S. The endocrinology of a naturally breeding population of white-crowned sparrow, Zonotrichia leucophrys pugetensis. Physiol. Zool. 1978, 51:188-205.
180. Wingfield J.C., Farner D.S. Endocrinology of reproduction in wild species. Avian Biology 1993, 163-327. Academic Press, San Diego. D.S. Farner, J. King, K. Parkes (Eds.).
181. Wingfield J.C., Goldsmith A.R. Plasma levels of prolactin and gonadal steroids in relation to multiple-brooding and renesting in free-living populations of the song sparrow, Melospiza melodia. Horm. Behav. 1990, 24:89-103.
182. Wingfield J.C., Hahn T.P. Testosterone and territorial behavior in sedentary and migratory sparrows. Anim. Behav. 1994, 47:77-89.
183. Wingfield J.C., Monk D. Behavioral and hormonal responses of male song sparrows to estradiol-treated females during the non-breeding season. Horm. Behav. 1994, 28:146-154.
184. Wingfield J.C., Wada M. Male-male interactions increase both luteinizing hormone and testosterone in the song sparrow, Melospiza melodia: Specificity, time course and possible neural pathways. J. Comp. Physiol. A 1989, 166:189-194.
185. Wingfield J.C., Ball G.F., Dufty A.M., Hegner R.E., Ramenofsky M. Testosterone and aggression in birds: Tests of the "challenge hypothesis". Am. Sci. 1987, 75:602-608.
186. Wingfield J.C., Hegner R.F., Dufty A.M.J., Ball G.F. The challenge hypothesis: Theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am. Nat. 1990, 136:829-846.
187. Wingfield J.C., Lynn S.E., Soma K.K. Avoiding the 'costs' of testosterone: Ecological bases of hormone-behavior interactions. Brain Behav. Evol. 2001, 57:239-251.
188. Wynne-Edwards K.E. Hormonal changes in mammalian fathers. Horm. Behav. 2001, 40:139-145.
189. Yang E.J., Wilczynski W. Social experience organizes parallel networks in sensory and limbic forebrain. Dev. Neurobiol. 2007, 67:285-303.
190. Zera A.J., Harshman L.G. The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 2001, 32:95-126.