Journal of Ornithology

, Volume 148, Supplement 1, pp 17–26 | Cite as

Hormones and the development of sex differences in behavior

  • Elizabeth Adkins-Regan


Birds exhibit striking diversity in behavioral sex differences. A necessary complement to the study of the ecology and evolution of these sex differences is discovering the proximate physiological mechanisms for their development (sexual differentiation) and adult expression. Experiments with Japanese quail (Coturnix japonica) have shown that sex differences in crowing, strutting, and sexual receptivity are produced partly or largely by hormonal dimorphism in adulthood (activational effects of sex steroid hormones), whereas the sex difference in copulatory mounting is produced by permanent actions of sex steroids occurring early in development, during the embryonic period in this precocial species (organizational effects). Experiments with zebra finches (Taeniopygia guttata), an altricial species, have revealed organizational effects on singing and mating that occur after hatching. In both species, sex differences in whether birds are interested in females vs. males are produced by organizational rather than activational effects. Results of experimental manipulations of sex steroid actions in juvenile zebra finches suggest hormonal regulation of the onset of interest in the opposite sex as sexual maturity is reached. Zebra finches are socially monogamous and permanently paired across breeding attempts. Experimental reduction of sex steroid actions had no effect on pairing success in either sex. The regulation of adult pair formation by sex hormones is more likely to occur in species that pair seasonally. The concepts of organization and activation and the results of these experiments raise a number of questions and are a potential source of hypotheses about developmental changes responsible for the evolution of species diversity in sex differences.


Japanese quail Pair formation Sex steroid Sexual differentiation Zebra finch 



The author’s research was supported by the U.S. National Science Foundation. The contributions of the following people to the research reviewed here are gratefully acknowledged: Norman Adler, Mary Ascenzi, Sunayana Banerjee, Tim Van Deusen, James Goodson, Alan Krakauer, Cary Leung, Viveka Mansukhani, Mary Ann Ottinger, Tiffany Robinson, Cynthia Seiwert, Maggie Smith, Richmond Thompson, Michelle Tomaszycki, Juli Wade, and Sharlene Yang.


  1. Adkins EK (1975) Hormonal basis of sexual differentiation in the Japanese quail. J Comp Physiol Psychol 89:61–71PubMedCrossRefGoogle Scholar
  2. Adkins EK (1976) Embryonic exposure to an antiestrogen masculinizes behavior of female quail. Physiol Behav 17:357–359PubMedCrossRefGoogle Scholar
  3. Adkins EK (1979) Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain: critical period and dose-response relationships. Neuroendocrinology 29:178–185PubMedCrossRefGoogle Scholar
  4. Adkins EK, Adler NT (1972) Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol 81:27–36PubMedCrossRefGoogle Scholar
  5. Adkins-Regan E (1988) Sex hormones and sexual orientation in animals. Psychobiol 16:335–347Google Scholar
  6. Adkins-Regan E (2005a) Hormones and animal social behavior. Princeton University Press, PrincetonGoogle Scholar
  7. Adkins-Regan E (2005b) Tactile contact is required for early estrogen treatment to alter the sexual partner preference of female zebra finches. Horm Behav 48:180–186PubMedCrossRefGoogle Scholar
  8. Adkins-Regan E, Ascenzi M (1987) Social and sexual behaviour of male and female zebra finches treated with oestradiol during the nestling period. Anim Behav 35:1100–1112CrossRefGoogle Scholar
  9. Adkins-Regan E, Ascenzi M (1990) Sexual differentiation of behavior in the zebra finch: effect of early gonadectomy or androgen treatment. Horm Behav 24:114–127PubMedCrossRefGoogle Scholar
  10. Adkins-Regan E, Krakauer A (2000) Removal of adult males from the rearing environment increases preference for same sex partners in the zebra finch (Taeniopygia guttata). Anim Behav 60:47–53PubMedCrossRefGoogle Scholar
  11. Adkins-Regan E, Leung CH (2006) Sex steroids modulate changes in social and sexual preference during juvenile development in zebra finches. Horm Behav 50:772–778PubMedCrossRefGoogle Scholar
  12. Adkins-Regan E, Robinson TM (1993) Sex differences in aggressive behavior in zebra finches (Poephila guttata). J Comp Psychol 107:223–229CrossRefGoogle Scholar
  13. Adkins-Regan E, Wade J (2001) Masculinized sexual partner preference in female zebra finches with sex-reversed gonads. Horm Behav 39:22–28PubMedCrossRefGoogle Scholar
  14. Adkins-Regan E, Abdelnabi M, Mobarak M, Ottinger M A (1990) Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endocrinol 78:93–109PubMedCrossRefGoogle Scholar
  15. Adkins-Regan E, Mansukhani V, Seiwert C, Thompson R (1994) Sexual differentiation of brain and behavior in the zebra finch: critical periods for effects of early estrogen treatment. J Neurobiol 25:865–877PubMedCrossRefGoogle Scholar
  16. Adkins-Regan E, Yang S, Mansukhani V (1996) Behavior of male and female zebra finches treated with an estrogen synthesis inhibitor as nestlings. Behaviour 133:847–862CrossRefGoogle Scholar
  17. Arnold AP (1980) Effects of androgens on volumes of sexually dimorphic brain regions in the zebra finch. Brain Res 185:441–444PubMedCrossRefGoogle Scholar
  18. Arnold AP (2002) Concepts of genetic and hormonal induction of vertebrate sexual differentiation in the twentieth century, with special reference to the brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol 4. Academic Elsevier, Amsterdam, pp 105–136Google Scholar
  19. Arnold AP, Schlinger BA (1993) Sexual differentiation of brain and behavior: the zebra finch is not just a flying rat. Brain Behav Evol 42:231–241PubMedCrossRefGoogle Scholar
  20. Balthazart J, Adkins-Regan E (2002) Sexual differentiation of brain and behavior in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol 4. Academic Elsevier, Amsterdam, pp 223–301Google Scholar
  21. Balthazart J, Delville Y, Sulon J, Hendrick J C (1986) Plasma levels of luteinizing hormone and of five steroids in photostimulated, castrated and testosterone-treated male and female Japanese quail (Coturnix coturnix japonica). Gen Endocrinol 5:31–36Google Scholar
  22. Balthazart J, Castagna C, Ball GF (1997) Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav Neurosci 111:381–397PubMedCrossRefGoogle Scholar
  23. Baum MJ (2006) Mammalian animal models of psychosexual differentiation: when is ‘translation’ to the human situation possible? Horm Behav 50:579–588PubMedCrossRefGoogle Scholar
  24. Beach FA, Inman NG (1965) Effects of castration and androgen replacement on mating in male quail. Proc Natl Acad Sci USA 54:1426–1431PubMedCrossRefGoogle Scholar
  25. Brenowitz EA, Arnold AP (1986) Interspecific comparisons of the size of neural song control regions and song complexity in duetting birds: evolutionary implications. J Neurosci 6:2875–2879PubMedGoogle Scholar
  26. Collins SA, Hubbard C, Houtman AM (1994) Female mate choice in the zebra finch – the effect of male beak colour and male song. Behav Ecol Sociobiol 35:21–25Google Scholar
  27. del Hoyo J (1994) Family Cracidae. In: del Hoyo J, Elliott A, Sargatal J et al. (eds) Handbook of the birds of the world, vol 2. Lynx Edicions, Barcelona, pp 310–341Google Scholar
  28. Eens M, Pinxten R (2000) Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behav Proc 51:135–147CrossRefGoogle Scholar
  29. Farabaugh SM (1982) The ecological and social significance of duetting. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds, vol 2. Academic, New York, pp 85–124Google Scholar
  30. Fivizzani AJ, Oring LW, El Halawani ME, Schlinger BA (1990) Hormonal basis of male parental care and female intersexual competition in sex-role reversed birds. In: Wada M, Ishii S, Scanes CG (eds) Endocrinology of birds: molecular to behavioral. Japan Scientific Societies Press/Springer, Tokyo/Berlin, pp 273–286Google Scholar
  31. Garamszegi LZ, Pavlova DZ, Eens M, Møller AP (2006) The evolution of song in female birds in Europe. Behav Ecol 18:86–96CrossRefGoogle Scholar
  32. Grisham W, Arnold AP (1995) A direct comparison of the masculinizing effects of testosterone, androstenedione, estrogen, and progesterone on the development of the zebra finch song system. J Neurobiol 26:163–170PubMedCrossRefGoogle Scholar
  33. Gurney ME, Konishi M (1980) Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science 208:1380–1383PubMedCrossRefGoogle Scholar
  34. Halldin K (2005) Impact of endocrine disrupting chemicals on sexual differentiation in Japanese quail. Neuroendocrine and behavioral consequences of embryonic exposure to endocrine disrupting chemicals. In: Dawson A, Sharp PJ (eds) Functional avian endocrinology. Narosa Publishing House, New Delhi, pp 299–309Google Scholar
  35. Jones KM, Monaghan P, Nager RG (2001) Male mate choice and female fecundity in zebra finches. Anim Behav 62:1021–1026CrossRefGoogle Scholar
  36. Levin R (1996) Song behaviour and reproductive strategies in a duetting wren, Thryothorus nigricapillus: I. Removal experiments. Anim Behav 52:1093–1106CrossRefGoogle Scholar
  37. MacDougall-Shackleton SA, Ball GF (1999) Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci 22:432–436PubMedCrossRefGoogle Scholar
  38. Madge S, McGowan P (2002) Pheasants, partridges, and grouse. Princeton University Press, PrincetonGoogle Scholar
  39. Mann NI, Barker FK, Graves JA, Dingess-Mann KA, Slater PJB (2006) Molecular data delineate four genera of “Thryothorus” wrens. Mol Phylogenet Evol 40:750–759PubMedCrossRefGoogle Scholar
  40. Mansukhani V, Adkins-Regan E, Yang S (1996) Sexual partner preference in female zebra finches: the role of early hormones and social environment. Horm Behav 30:506–513PubMedCrossRefGoogle Scholar
  41. McGlothlin JW, Neudorf DL, Casto JM, Nolan V, Ketterson ED (2004) Elevated testosterone reduces choosiness in female dark-eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? Proc R Soc Lond B 271:1377–1384CrossRefGoogle Scholar
  42. Nealen PM, Perkel DJ (2000) Sexual dimorphism in the song system of the Carolina wren Thryothorus ludovicianus. J Comp Neurol 418:346–360PubMedCrossRefGoogle Scholar
  43. Nelson RJ (2005) An introduction to behavioral endocrinology, 3rd edn. Sinauer, SunderlandGoogle Scholar
  44. Ottinger MA, Pitts S, Abdelnabi MA (2001) Steroid hormones during embryonic development in Japanese quail: plasma, gonadal, and adrenal levels. Poultry Sci 80:795–799Google Scholar
  45. Ottinger MA, Quinn MJ, Lavoie E, Abdelnabi MA, Thompson N, Hazelton J, McKernan M, Wu JM, Henry PFP, Viglietti-Panzica C, Panzica GC (2005) Neuroendocrine and behavioral consequences of embryonic exposure to endocrine disrupting chemicals. In: Dawson A, Sharp PJ (eds) Functional avian endocrinology. Narosa Publishing House, New Delhi, pp 271–284Google Scholar
  46. Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinol 65:369–382CrossRefGoogle Scholar
  47. Sayag N, Snapir N, Robinzon B, Arnon E, el Halawani ME, Grimm VE (1989) Embryonic sex steroids affect mating behavior and plasma LH in adult chickens. Physiol Behav 45:1107–1112PubMedCrossRefGoogle Scholar
  48. Schlinger BA, London SE (2006) Neurosteroids and the songbird model system. J Exp Zool 305:743–748CrossRefGoogle Scholar
  49. Schlinger BA, Fivizzani AJ, Callard GV (1989) Aromatase, 5α- and 5β-reductase in brain, pituitary and skin of the sex-role reversed Wilson’s phalarope. J Endocrinol 122:573–581PubMedCrossRefGoogle Scholar
  50. Schumacher M, Balthazart J (1983) The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol Behav 30:335–339PubMedCrossRefGoogle Scholar
  51. Schumacher M, Sulon J, Balthazart J (1988) Changes in serum concentrations of steroids during embryonic and post-hatching development of male and female Japanese quail (Coturnix coturnix japonica). J Endocrinol 118:127–134PubMedGoogle Scholar
  52. Tanabe Y, Nakamura T, Fujioka K, Doi O (1979) Production and secretion of sex steroid hormones by the testes, the ovary, and the adrenal glands of embryonic and young chickens (Gallus domesticus). Gen Comp Endocrinol 39:26–33PubMedCrossRefGoogle Scholar
  53. Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433Google Scholar
  54. Tomaszycki ML, Banerjee SB, Adkins-Regan E (2006) The role of sex steroids in courtship, pairing and pairing behaviors in the socially monogamous zebra finch. Horm Behav 50:141–147PubMedCrossRefGoogle Scholar
  55. Wade J (1999) Sexual dimorphisms in avian and reptilian courtship: two systems that do not play by mammalian rules. Brain Behav Evol 54:15–27PubMedCrossRefGoogle Scholar
  56. Wade J, Tang YP, Peabody C, Tempelman RJ (2005) Enhanced gene expression in the forebrain of hatchling and juvenile male zebra finches. J Neurobiol 64:224–238PubMedCrossRefGoogle Scholar
  57. Williams H, Kilander K, Sotanski ML (1993) Untutored song, reproductive success and song learning. Anim Behav 45:695–705CrossRefGoogle Scholar
  58. Wilson JA, Glick B (1970) Ontogeny of mating behavior in the chicken. Am J Physiol 218:951–955Google Scholar
  59. Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 9. Academic, London, pp 164–328Google Scholar
  60. Yazaki Y, Matsushima T, Aoki K (1999) Testosterone modulates stimulation-induced calling behavior in Japanese quails. J Comp Physiol A 184:13–19PubMedCrossRefGoogle Scholar
  61. Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2007

Authors and Affiliations

  1. 1.Cornell UniversityIthacaUSA

Personalised recommendations