Archives of Sexual Behavior

, Volume 46, Issue 6, pp 1583–1592 | Cite as

Prenatal Influences on Human Sexual Orientation: Expectations versus Data

  • S. Marc Breedlove
Target Article


In non-human vertebrate species, sexual differentiation of the brain is primarily driven by androgens such as testosterone organizing the brains of males in a masculine fashion early in life, while the lower levels of androgen in developing females organize their brains in a feminine fashion. These principles may be relevant to the development of sexual orientation in humans, because retrospective markers of prenatal androgen exposure, namely digit ratios and otoacoustic emissions, indicate that lesbians, on average, were exposed to greater prenatal androgen than were straight women. Thus, the even greater levels of prenatal androgen exposure experienced by fetal males may explain why the vast majority of them grow up to be attracted to women. However, the same markers indicate no significant differences between gay and straight men in terms of average prenatal androgen exposure, so the variance in orientation in men cannot be accounted for by variance in prenatal androgen exposure, but may be due to variance in response to prenatal androgens. These data contradict several popular notions about human sexual orientation. Sexual orientation in women is said to be fluid, sometimes implying that only social influences in adulthood are at work, yet the data indicate prenatal influences matter as well. Gay men are widely perceived as under-masculinized, yet the data indicate they are exposed to as much prenatal androgen as straight men. There is growing sentiment to reject “binary” conceptions of human sexual orientations, to emphasize instead a spectrum of orientations. Yet the data indicate that human sexual orientation is sufficiently polarized that groups of lesbians, on average, show evidence of greater prenatal androgen exposure than groups of straight women, while groups of gay men have, on average, a greater proportion of brothers among their older siblings than do straight men.


Sexual orientation Testosterone Androgens Birth order Digit ratios Otoacoustic emissions 



This article was funded by NIH Grant R21MH104780.

Compliance with Ethical Standards

Conflict of interest

The author declares no conflict of interest.


  1. Allen, L. S., & Gorski, R. A. (1991). Sexual dimorphism of the anterior commissure and massa intermedia of the human brain. Journal of Comparative Neurology, 312(1), 97–104.CrossRefPubMedGoogle Scholar
  2. Allen, L. S., Hines, M., Shryne, J. E., & Gorski, R. A. (1989). Two sexually dimorphic cell groups in the human brain. Journal of Neuroscience, 9, 497–506.PubMedGoogle Scholar
  3. Bailey, J. M., Vasey, P. L., Diamond, L. M., Breedlove, S. M., Vilain, E., & Epprecht, M. (2016). Sexual orientation, controversy, and science. Psychological Science in the Public Interest, 17(2), 45–101. doi: 10.1177/1529100616637616.CrossRefPubMedGoogle Scholar
  4. Baker, M. (2016). 1,500 scientists lift the lid on reproducibility. Nature, 533(7604), 452–454. doi: 10.1038/533452a.CrossRefPubMedGoogle Scholar
  5. Berenbaum, S. A., Bryk, K. K., Nowak, N., Quigley, C. A., & Moffat, S. (2009). Fingers as a marker of prenatal androgen exposure. Endocrinology, 150(11), 5119–5124.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blanchard, R. (1997). Birth order and sibling sex ration in homosexual versus heterosexual males and females. Annual Review Sex Research, 8, 27–67.Google Scholar
  7. Blanchard, R., & Bogaert, A. (1996). Homosexuality in men and number of older brothers. American Journal of Psychiatry, 153(1), 27–31.CrossRefPubMedGoogle Scholar
  8. Blanchard, R., Cantor, J. M., Bogaert, A. F., Breedlove, S. M., & Ellis, L. (2006). Interaction of fraternal birth order and handedness in the development of male homosexuality. Hormones and Behavior, 49(3), 405–414.CrossRefPubMedGoogle Scholar
  9. Blanchard, R., Zucker, K. J., Siegelman, M., Dickey, R., & Klassen, P. (1998). The relation of birth order to sexual orientation in men and women. Journal of Biosocial Science, 30, 511–519.CrossRefPubMedGoogle Scholar
  10. Block, J. H. (1983). Differential premises arising from differential socialization of the sexes: Some conjectures. Child Development, 54(6), 1335–1354.CrossRefPubMedGoogle Scholar
  11. Bogaert, A. F. (2006). Biological versus nonbiological older brothers and men’s sexual orientation. Proceedings of the National Academy of Sciences of the United States of America, 103(28), 10771–10774. doi: 10.1073/pnas.0511152103.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bogaert, A. F., & Hershberger, S. (1999). The relation between sexual orientation and penile size. Archives of Sexual Behavior, 28(3), 213–221.CrossRefPubMedGoogle Scholar
  13. Bogin, B. (1997). Evolutionary hypotheses about human childhood. Yearbook of Physical Anthropology, 40, 60–89.Google Scholar
  14. Breedlove, S. M., & Arnold, A. P. (1980). Hormone accumulation in a sexually dimorphic motor nucleus in the rat spinal cord. Science, 210, 564–566.CrossRefPubMedGoogle Scholar
  15. Brown, W. M., Finn, C. J., & Breedlove, S. M. (2002a). Sexual dimorphism in digit-length ratios of laboratory mice. Anatomical Record, 267(3), 231–234.CrossRefPubMedGoogle Scholar
  16. Brown, W. M., Finn, C. J., Cooke, B. M., & Breedlove, S. M. (2002b). Differences in finger length ratios between self-identified “butch” and “femme” lesbians. Archives of Sexual Behavior, 31(1), 123–127.CrossRefPubMedGoogle Scholar
  17. Brown, W. M., Hines, M., Fane, B. A., & Breedlove, S. M. (2002c). Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Hormones and Behavior, 42(4), 380–386.CrossRefPubMedGoogle Scholar
  18. Byne, W. (1998). The medial preoptic and anterior hypothalamic regions of the rhesus monkey: Cytoarchitectonic comparison with the human and evidence for sexual dimorphism. Brain Research, 793(1–2), 346–350.CrossRefPubMedGoogle Scholar
  19. Campbell, A. (2013). A mind of her own: The evolutionary psychology of women (2nd ed.). New York: Oxford University Press.CrossRefGoogle Scholar
  20. Clark, A. S., Davis, L. A., & Roy, E. J. (1985). A possible physiological basis for the dud-stud phenomenon. Hormones and Behavior, 19(2), 227–230.CrossRefPubMedGoogle Scholar
  21. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum Associates.Google Scholar
  22. Colapinto, J. (1997, 11 December). The true story of John/Joan. Rolling Stone, pp. 54–97.Google Scholar
  23. Colapinto, J. (2000). As nature made him: The boy who was raised as a girl. New York, NY: Harper Collins.Google Scholar
  24. Cooke, B. M., Chowanadisai, W., & Breedlove, S. M. (2000). Post-weaning social isolation of male rats reduces the volume of the medial amygdala and leads to deficits in adult sexual behavior. Behavioural Brain Research, 117(1–2), 107–113.CrossRefPubMedGoogle Scholar
  25. Cooke, B. M., Tabibnia, G., & Breedlove, S. M. (1999). A brain sexual dimorphism controlled by adult circulating androgens. Proceedings of the National Academy of Sciences of the United States of America, 96(13), 7538–7540.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Csatho, A., Osvath, A., Bicsak, E., Karadi, K., Manning, J., & Kallai, J. (2003). Sex role identity related to the ratio of second to fourth digit length in women. Biological Psychology, 62(2), 147–156.CrossRefPubMedGoogle Scholar
  27. Damassa, D. A., Smith, E. R., Tennent, B., & Davidson, J. M. (1977). The relationship between circulating testosterone levels and male sexual behavior in rats. Hormones and Behavior, 8, 275–286.CrossRefPubMedGoogle Scholar
  28. De Jonge, F. H., Louwerse, A. L., Ooms, M. P., Evers, P., Endert, E., & Van de Poll, N. E. (1989). Lesions of the SDN–POA inhibit sexual behavior of male Wistar rats. Brain Research Bulletin, 23, 483–492.CrossRefPubMedGoogle Scholar
  29. Diamond, L. M. (2008a). Female bisexuality from adolescence to adulthood: Results from a 10-year longitudinal study. Developmental Psychology, 44, 5–14.CrossRefPubMedGoogle Scholar
  30. Diamond, L. M. (2008b). Sexual fluidity: Understanding women’s love and desire. Cambridge, MA: Harvard University Press.Google Scholar
  31. Diamond, L. M., & Rosky, C. J. (2016). Scrutinizing immutability: Research on sexual orientation and U.S. legal advocacy for sexual minorities. Journal of Sex Research, 53(4–5), 363–391. doi: 10.1080/00224499.2016.1139665.CrossRefPubMedGoogle Scholar
  32. Diamond, M., & Sigmundson, H. (1997). Sex reassignment at birth. Long-term review and clinical implications. Archives of Pediatrics and Adolescent Medicine, 151(3), 298–304.CrossRefPubMedGoogle Scholar
  33. Dickman, S. (1997). HOX gene links limb, genital defects. Science, 275(5306), 1568.CrossRefPubMedGoogle Scholar
  34. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans (2nd ed.). New York: Oxford University Press.CrossRefGoogle Scholar
  35. Eaton, G. G., Goy, R. W., & Phoenix, C. H. (1973). Effects of testosterone treatment in adulthood on sexual behaviour of female pseudohermaphrodite rhesus monkeys. Nature New Biology, 242(117), 119–120.CrossRefPubMedGoogle Scholar
  36. Forger, N. G., & Breedlove, S. M. (1986). Sexual dimorphism in human and canine spinal cord: Role of early androgen. Proceedings of the National Academy of Sciences, 83, 7527–7531.CrossRefGoogle Scholar
  37. Galis, F., Ten Broek, C. M., Van Dongen, S., & Wijnaendts, L. C. (2010). Sexual dimorphism in the prenatal digit ratio (2D:4D). Archives of Sexual Behavior, 39, 57–62.CrossRefPubMedGoogle Scholar
  38. Gerressu, M., Mercer, C. H., Graham, C. A., Wellings, K., & Johnson, A. M. (2008). Prevalence of masturbation and associated factors in a British national probability survey. Archives of Sexual Behavior, 37(2), 266–278. doi: 10.1007/s10508-006-9123-6.CrossRefPubMedGoogle Scholar
  39. Golombok, S., & Fivush, R. (1994). Gender development. New York: Cambridge University Press.Google Scholar
  40. Gorski, R. A., Harlan, R. E., Jacobson, C. D., Shryne, J. E., & Southam, A. M. (1980). Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. Journal Comparative Neurology, 193, 529–539.CrossRefGoogle Scholar
  41. Goy, R. W., & Phoenix, C. H. (1972). The effects of testosterone propionate administered before birth on the development of behavior in genetic female rhesus monkeys. UCLA Forum in Medical Sciences, 15, 193–201.PubMedGoogle Scholar
  42. Grimbos, T., Dawood, K., Burriss, R. P., Zucker, K. J., & Puts, D. A. (2010). Sexual orientation and the second to fourth finger length ratio: A meta-analysis in men and women. Behavioral Neuroscience, 124(2), 278–287. doi: 10.1037/a0018764.CrossRefPubMedGoogle Scholar
  43. Grunt, J. A., & Young, W. C. (1953). Consistency of sexual behavior patterns in individual male guinea pigs following castration and androgen therapy. Journal of Comparative and Physiological Psychology, 46(2), 138–144.CrossRefPubMedGoogle Scholar
  44. Guiso, L., Monte, F., Sapienza, P., & Zingales, L. (2008). Diversity. Culture, gender, and math. Science, 320(5880), 1164–1165. doi: 10.1126/science.1154094.CrossRefPubMedGoogle Scholar
  45. Gurney, M. E. (1982). Behavioral correlates of sexual differentiation in the zebra finch song system. Brain Research, 231, 153–172.CrossRefPubMedGoogle Scholar
  46. Hall, L. S., & Love, C. T. (2003). Finger-length ratios in female monozygotic twins discordant for sexual orientation. Archives of Sexual Behavior, 32(1), 23–28.CrossRefPubMedGoogle Scholar
  47. Hamer, D. D., Hu, S., Magnuson, V. L., Hu, N., & Pattatucci, A. M. L. (1993). A linkage between DNA markers on the X chromosome and male sexual orientation. Science, 261, 321–327.CrossRefPubMedGoogle Scholar
  48. Hiraishi, K., Sasaki, S., Shikishima, C., & Ando, J. (2012). The second to fourth digit ratio (2D:4D) in a Japanese twin sample: Heritability, prenatal hormone transfer, and association with sexual orientation. Archives of Sexual Behavior, 41(3), 711–724. doi: 10.1007/s10508-011-9889-z.CrossRefPubMedGoogle Scholar
  49. Honekopp, J., & Watson, S. (2010). Meta-analysis of digit ratio 2D:4D shows greater sex difference in the right hand. American Journal of Human Biology, 22(5), 619–630. doi: 10.1002/ajhb.21054.CrossRefPubMedGoogle Scholar
  50. Kraemer, B., Noll, T., Delsignore, A., Milos, G., Schnyder, U., & Hepp, U. (2006). Finger length ratio (2D:4D) and dimensions of sexual orientation. Neuropsychobiology, 53(4), 210–214.CrossRefPubMedGoogle Scholar
  51. LeVay, S. (1991). A difference in hypothalamic structure between heterosexual and homosexual men. Science, 253, 1034–1037.CrossRefPubMedGoogle Scholar
  52. LeVay, S. (2016). Gay, straight, and the reason why: The science of sexual orientation. New York: Oxford University Press.Google Scholar
  53. Lippa, R. A. (2008). Sex differences and sexual orientation differences in personality: Findings from the BBC Internet survey. Archives of Sexual Behavior, 37(1), 173–187. doi: 10.1007/s10508-007-9267-z.CrossRefPubMedGoogle Scholar
  54. Malas, M. A., Dogan, S., Evcil, E. H., & Desdicioglu, K. (2006). Fetal development of the hand, digits and digit ratio (2D:4D). Early Human Development, 82(7), 469–475.CrossRefPubMedGoogle Scholar
  55. Manning, J. T., Scutt, D., Wilson, J., & Lewis-Jones, D. I. (1998). The ratio of 2nd–4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction, 13(11), 3000–3004.CrossRefPubMedGoogle Scholar
  56. Martin, C. L., & Ruble, D. N. (2010). Patterns of gender development. Annual Review of Psychology, 61, 353–381. doi: 10.1146/annurev.psych.093008.100511.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Maxwell, S. E., Lau, M. Y., & Howard, G. S. (2015). Is psychology suffering from a replication crisis? What does “failure to replicate” really mean? American Psychologist, 70(6), 487–498. doi: 10.1037/a0039400.CrossRefPubMedGoogle Scholar
  58. McFadden, D., & Champlin, C. A. (2000). Comparison of auditory evoked potentials in heterosexual, homosexual, and bisexual males and females. Journal of the Association for Research in Otolaryngology, 1(1), 89–99.CrossRefPubMedPubMedCentralGoogle Scholar
  59. McFadden, D., & Pasanen, E. G. (1998). Comparison of the auditory systems of heterosexuals and homosexuals: Click-evoked otoacoustic emissions. Proceedings of the National Academy of Sciences of the United States of America, 95(5), 2709–2713.CrossRefPubMedPubMedCentralGoogle Scholar
  60. McFadden, D., & Pasanen, E. G. (1999). Spontaneous otoacoustic emissions in heterosexuals, homosexuals, and bisexuals. Journal of the Acoustic Society of America, 105(4), 2403–2413.CrossRefGoogle Scholar
  61. McFadden, D., & Shubel, E. (2002). Relative lengths of fingers and toes in human males and females. Hormones and Behavior, 42(4), 492–500.CrossRefPubMedGoogle Scholar
  62. Meyer-Bahlburg, H. F. L., Dolezal, C., Baker, S. W., & New, M. I. (2008). Sexual orientation in women with classical or non-classical congenital adrenal hyperplasia as a function of degree of prenatal androgen excess. Archives of Sexual Behavior, 37(1), 85–99. doi: 10.1007/s10508-007-9265-1.CrossRefPubMedGoogle Scholar
  63. Money, J., & Ehrhardt, A. A. (1972). Man & woman, boy & girl: Differentiation and dimorphism of gender identity from conception to maturity. Baltimore: Johns Hopkins University Press.Google Scholar
  64. Money, J., Schwartz, M., & Lewis, V. (1984). Adult heterosexual status and fetal hormonal masculinization and demasculinization: 46XX congenital virilizing hyperplasia and 46XY androgen insensitivity compared. Psychoneuroendocrinology, 9, 405–414.CrossRefPubMedGoogle Scholar
  65. Morishima, A., Grumbach, M. M., Simpson, E. R., Fisher, C., & Qin, K. (1995). Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. Journal of Clinical Endocrinology and Metabolism, 80(12), 3689–3698.PubMedGoogle Scholar
  66. Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2004). Sexual differentiation of the vertebrate nervous system. Nature Neuroscience, 7(10), 1034–1039.CrossRefPubMedGoogle Scholar
  67. Mustanski, B. S., Chivers, M. L., & Bailey, J. M. (2002). A critical review of recent biological research on human sexual orientation. Annual Review of Sex Research, 13, 89–140.PubMedGoogle Scholar
  68. Nedoma, K., & Freund, K. (1961). Somatosexual findings in homosexual men. Ceskoslovenska Psychiatre, 57, 100–103.Google Scholar
  69. Nottebohm, F., & Arnold, A. (1976). Sexual dimorphism in vocal control areas of the songbird brain. Science, 194, 211–213.CrossRefPubMedGoogle Scholar
  70. Okten, A., Kalyoncu, M., & Yaris, N. (2002). The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Human Development, 70(1–2), 47–54.CrossRefPubMedGoogle Scholar
  71. Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65, 369–382.CrossRefPubMedGoogle Scholar
  72. Prior, L., Bordet, S., Trifiro, M. A., Mhatre, A., Kaufman, M., Pinsky, L., … Liao, S. (1992). Replacement of arginine 773 by cysteine or histidine in the human androgen receptor causes complete androgen insensitivity with different receptor phenotypes. American Journal Human Genetics, 51, 143–155.Google Scholar
  73. Putz, D. A., Gaulin, S. J., Sporter, R. J., & McBurney, D. H. (2004). Sex hormones and finger length: What does 2D:4D indicate? Evolution and Human Behavior, 25, 182–199.CrossRefGoogle Scholar
  74. Rahman, Q. (2005). Fluctuating asymmetry, second–fourth finger length ratios and human sexual orientation. Psychoneuroendocrinology, 30(4), 382–391. doi: 10.1016/j.psyneuen.2004.10.006.CrossRefPubMedGoogle Scholar
  75. Rahman, Q., & Wilson, G. D. (2003). Sexual orientation and the 2nd–4th finger length ratio: Evidence for organising effects of sex hormones or developmental instability? Psychoneuroendocrinology, 28(3), 288–303.CrossRefPubMedGoogle Scholar
  76. Reiner, W. G. (2004). Psychosexual development in genetic males assigned female: The cloacal exstrophy experience. Child and Adolescent Psychiatric Clinics of North America, 13(3), 657–674. doi: 10.1016/j.chc.2004.02.009.CrossRefPubMedGoogle Scholar
  77. Reiner, W. G., & Gearhart, J. P. (2004). Discordant sexual identity in some genetic males with cloacal exstrophy assigned to female sex at birth. New England Journal of Medicine, 350(4), 333–341. doi: 10.1056/NEJMoa022236.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Rieger, G., Linsenmeier, J. A., Gygax, L., & Bailey, J. M. (2008). Sexual orientation and childhood gender nonconformity: Evidence from home videos. Developmental Psychology, 44(1), 46–58. doi: 10.1037/0012-1649.44.1.46.CrossRefPubMedGoogle Scholar
  79. Roselli, C. E., Larkin, K., Resko, J. A., Stellflug, J. N., & Stormshak, F. (2004). The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology, 145(2), 478–483. doi: 10.1210/en.2003-1098.CrossRefPubMedGoogle Scholar
  80. Sanders, A. R., Martin, E. R., Beecham, G. W., Guo, S., Dawood, K., Rieger, G., … Bailey, J. M. (2015). Genome-wide scan demonstrates significant linkage for male sexual orientation. Psychological Medicine, 45(7), 1379–1388. doi: 10.1017/S0033291714002451.
  81. Singh, D., Vidaurri, M., Zambarano, R. J., & Dabbs, J. M., Jr. (1999). Lesbian erotic role identification: Behavioral, morphological, and hormonal correlates. Journal of Personality and Social Psychology, 76(6), 1035–1049.CrossRefPubMedGoogle Scholar
  82. Swaab, D. F., & Fliers, E. (1985). A sexually dimorphic nucleus in the human brain. Science, 228, 1112–1115.CrossRefPubMedGoogle Scholar
  83. Tortorice, J. L. (2002). Written on the body: Butch vs. femme lesbian gender identity and biological correlates of low digit ratio. New Brunswick, NJ: Rutgers University.Google Scholar
  84. Wallien, M. S., Zucker, K. J., Steensma, T. D., & Cohen-Kettenis, P. T. (2008). 2D:4D finger–length ratios in children and adults with gender identity disorder. Hormones and Behavior, 54(3), 450–454. doi: 10.1016/j.yhbeh.2008.05.002.CrossRefPubMedGoogle Scholar
  85. Williams, T. J., Pepitone, M. E., Christensen, S. E., Cooke, B. M., Huberman, A. D., Breedlove, N. J., … Breedlove, S. M. (2000). Finger–length ratios and sexual orientation. Nature, 404(6777), 455–456.Google Scholar
  86. Wudy, S. A., Dorr, H. G., Solleder, C., Djalali, M., & Homoki, J. (1999). Profiling steroid hormones in amniotic fluid of midpregnancy by routine stable isotope dilution/gas chromatography–mass spectrometry: Reference values and concentrations in fetuses at risk for 21-hydroxylase deficiency. Journal of Clinical Endocrinology and Metabolism, 84(8), 2724–2728.PubMedGoogle Scholar
  87. Zheng, Z., & Cohn, M. J. (2011). Developmental basis of sexually dimorphic digit ratios. Proceedings of the National Academy of Sciences of the United States of America, 108(39), 16289–16294. doi: 10.1073/pnas.1108312108.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Neuroscience Program and Departments of Psychology, Integrative BiologyMichigan State UniversityEast LansingUSA

Personalised recommendations