Prenatal testosterone transfer

Prenatal Testosterone Transfer (also known as prenatal androgen transfer or prenatal hormone transfer) refers to the phenomenon in which testosterone synthesized by a developing male fetus transfers to one or more developing fetuses within the womb and influences development. This typically results in the partial masculinization of specific aspects of female behavior, cognition, and morphology,[1] though some studies have found that testosterone transfer can cause an exaggerated masculinization in males.[2] There is strong evidence supporting the occurrence of prenatal testosterone transfer in rodents and other litter-bearing species,[1] such as pigs.[3] When it comes to humans, studies comparing dizygotic opposite-sex and same-sex twins suggest the phenomenon may occur, though the results of these studies are often inconsistent.[4][5]

Mechanisms of transfer

Testosterone is a steroid hormone; therefore it has the ability to diffuse through the amniotic fluid between fetuses.[6] In addition, hormones can transfer among fetuses through the mother's bloodstream.[7]

Consequences of testosterone transfer

During prenatal development, testosterone exposure is directly responsible for masculinizing the genitals[8] and brain structures.[9] This exposure leads to an increase in male-typical behavior.[10] When females are exposed to elevated levels of testosterone via transfer, the masculinization of a variety of traits have been reported to occur, including sexual behavior,[11] sex-typical play,[12] and spatial ability.[13]

Animal studies

Most animal studies are performed on rats or mice. In these studies, the amount of testosterone each individual fetus is exposed to depends on its intrauterine position (IUP). Each gestating fetus not at either end of the uterine horn is surrounded by either two males (2M), two females (0M), or one female and one male (1M). Development of the fetus varies widely according to its IUP.[1]

Mice

In mice, prenatal testosterone transfer causes higher blood concentrations of testosterone in 2M females when compared to 1M or 0M females.[6] This has a variety of consequences on later female behavior, physiology, and morphology.

Below is a table comparing physiological, morphological, and behavioral differences of 0M and 2M female mice.[1]

0M Female Mice 2M Female Mice
Physiology Lower fetal testosterone levels[14] Higher fetal testosterone levels[6]
Earlier vaginal opening[15] Later vaginal opening[16]
Less male offspring[17] More male offspring[17]
Mate and impregnated earlier[16] Mate and impregnated later[16]
Less sensitive to testosterone[18] More sensitive to testosterone[19]
Morphology Shorter anogenital distance[18] Longer anogenital distance[14]
Behavior Less likely to mount other females[20] More likely to mount other females[21]
Less aggressive[18] More aggressive[14]

Human studies

Studies involving humans often compare opposite-sex to same-sex dizygotic twins. Females of opposite-sex twin pairs are thought to have partially masculinized traits as a result of gestating along with a male. These studies test for a range of masculinized cognitive, morphological, physiological, and behavioral traits. Studies testing for differences in behavior (i.e. temperament) tend to yield inconsistent results,[22] while those testing perception and cognition are typically more consistent.[5] Though supporting evidence exists, whether or not prenatal testosterone transfer occurs in humans remains debatable.

Listed below are different types of opposite-sex versus same-sex twin tests used to determine whether prenatal testosterone transfer occurs in humans.

Tests of Behavior

Tests of Perception and Cognition

Tests of Physiology and Morphology

References

  1. 1 2 3 4 Ryan, B.C.; Vandenbergh, J.G. (2002). "Intrauterine position effects". Neuroscience & Biobehavioral Reviews 26 (6): 665–678. doi:10.1016/S0149-7634(02)00038-6. PMID 12479841.
  2. ↑ Clark, M.M.; Tucker, L.; Galfed, J.B.G. (1992). "Stud males and dud males: intrauterine position effects on the reproductive success of male gerbils". Animal Behavior 43 (2): 215–221. doi:10.1016/S0003-3472(05)80217-9.
  3. ↑ Rhode Parfet, K.A.; Lamberson, W.R., Ricke., A.R., Cantley, T.C., Ganjam, V.K., van Saal, F.S., Day, B.N. (1990). "Intrauterine position effects in male and female swine: Subsequent survivability, growth rate, morphology, and semen characteristics". Journal of Animal Science 68 (1): 179–185. PMID 2303395. Cite uses deprecated parameter |coauthors= (help)
  4. 1 2 3 Cohen-Bendahan, C.C.C.; Buitelaar, J.K., van Goozen, S.H.M., Orlebeke, J.F., Cohen-Kettenis, P.T. (2005a). "Is there an effect of prenatal testosterone on aggression and other behavioral traits? A study comparing same-sex and opposite-sex twin girls". Hormones and Behavior 47 (2): 230–237. doi:10.1016/j.yhbeh.2004.10.006. PMID 15664027. Cite uses deprecated parameter |coauthors= (help)
  5. 1 2 Tapp, A.L.; Mayberry, M.T.; Whitehouse, A.J.O. (2011). "Evaluating the twin testosterone transfer hypothesis: A review of the empirical evidence". Hormones and Behavior 60: 713–722. doi:10.1016/j.yhbeh.2011.08.011.
  6. 1 2 3 vom Saal, F.S.; Quadagno, D.M.; Even, M.D.; Keisler, L.W.; Keisler, D.H.; Khan, S. (1990). "Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions". Biol. Reprod. 43 (5): 751–761. doi:10.1095/biolreprod43.5.751. PMID 2291911.
  7. ↑ Gorodeski, G.I.; Sheean, L.A.; Utian, W.H. (1995). "Sex hormone modulation of flow velocity in the parametrial artery of the pregnant rat". Am. J. Physiol. 268 (3 Pt 2): R614–R624. PMID 7900903.
  8. ↑ Nelson, R.J. (2000). An Introduction to Behavioral Endocrinology, 2nd ed. Massachusetts: Sinauer Associates.
  9. ↑ Breedlove, S.M. (1994). "Sexual differentiation of the human nervous system". Annu. Rev. Psychol. 45: 389–418. doi:10.1146/annurev.ps.45.020194.002133. PMID 8135506.
  10. ↑ Goy, R.W.; Phoenix, C.H. (1972). "The effects of testosterone propionate administered before birth on the development of behaviour in genetic female rhesus monkeys". UCLA Forum Med. Sci. 15: 193–201. PMID 4628102.
  11. ↑ Wallen, K. (2005). "Hormonal influences on sexually differentiated behaviour in nonhuman primates". Front. Neuroendocrinol. 26 (1): 7–26. doi:10.1016/j.yfrne.2005.02.001. PMID 15862182.
  12. ↑ Meaney, M.J.; McEwen, B.S. (1986). "Testosterone implants into the amygdala during the neonatal period masculinise the social play of juvenile female ras". Brain Res. 398 (2): 324–328. doi:10.1016/0006-8993(86)91492-7. PMID 3801906.
  13. ↑ Chapman, E.; Baron-Cohen, S.; Auyeung, B.; Knickmeyer, R.; Taylor, K.; Hackett, G. (2006). "Fetal testosterone and empathy: evidence from the Empathy Quotient (EQ) and the "Reading the Mind in the Eyes" Test". Soc. Neurosci. 1 (2): 135–148. doi:10.1080/17470910600992239. PMID 18633782.
  14. 1 2 3 vom Saal, F.S.; Bronson, F.H. (1978). "In utero proximity of female mouse fetuses to males: effects on reproductive performance during later life". Biol. Reprod. 9: 842–853. doi:10.1095/biolreprod19.4.842. PMID 743525.
  15. ↑ McDermott, N.J.; Gandelman, R.; Reinisch, J.M. (1978). "Contiguity to male fetuses influences ano-genital distance and time of vaginal opening in mice". Physiol. Behav. 20 (5): 661–663. doi:10.1016/0031-9384(78)90261-5. PMID 567358.
  16. 1 2 3 vom Saal, F.S. (1989). "The production of and sensitivity to cues that delay puberty and prolong subsequent oestrous cycles in female mice are influenced by prior intrauterine position". J. Reprod. Fertil. 86 (2): 457–471. doi:10.1530/jrf.0.0860457. PMID 2760875.
  17. 1 2 Vandenbergh, J.G.; Huggett, C.L. (1995). "The anogenital distance index, a predictor of the intrauterine position effects on reproduction in female house mice". Lab. Anim. Sci. 45 (5): 567–573. PMID 8569159.
  18. 1 2 3 Gandelman, R.; vom Saal, F.S., Reinisch, J.M. (1977). "Contiguity to male fetuses affects morphology and behaviour of female mice". Nature 266 (5604): 722–724. doi:10.1038/266722a0. PMID 559940. Cite uses deprecated parameter |coauthors= (help)
  19. ↑ vom Saal, F.S.; Grant, W.M.; McMullen, C.W.; Laves, K.S. (1983). "High fetal estrogen concentrations: correlation with increased adult sexual activity and decreased aggression in male mice". Science 220 (4603): 1306–1309. doi:10.1126/science.6857252. PMID 6857252.
  20. ↑ Quadagno, D.M.; McQuitty, C.; McKee, J.; Koelliker, L.; Wolfe, G.; Johnson, D.C. (1987). "The effects of intrauterine position on competition and behavior in the mouse". Physiol. Behav. 41 (6): 639–642. doi:10.1016/0031-9384(87)90323-4. PMID 3441535.
  21. ↑ Rines, J.P.; vom Saal, F.S. (1984). "Fetal effects on sexual behavior and aggression in young and old female mice treated with estrogen and testosterone". Hormones and Behavior 18 (2): 117–129. doi:10.1016/0018-506X(84)90037-0. PMID 6539747. Cite uses deprecated parameter |coauthors= (help)
  22. ↑ Cohen-Bendahan, C.C.C.; van de Beek, C., Berenbaum, S.A. (2005b). "Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings". Neuroscience and Biobehavioral Reviews 29 (2): 353–384. doi:10.1016/j.neubiorev.2004.11.004. PMID 15811504. Cite uses deprecated parameter |coauthors= (help)
  23. ↑ Resnick, S.M.; Gottesman, I.I.; McGue, M. (1993). "Sensation seeking in opposite-sex twins: an effect of prenatal hormones?". Behavior Genetics 23 (4): 323–329. doi:10.1007/BF01067432. PMID 8240211.
  24. ↑ Rodgers, C.S.; Fagot, B.I.; Winebarger, A. (1998). "Gender-typed toy play in dizygotic twin pairs: a test of hormone transfer theory". Sex Roles 39 (3/4): 173–184. doi:10.1023/A:1018894219859.
  25. ↑ McFadden, D. (1993). "A masculinising effect on the auditory systems of human females having male co-twins". Proc. Natl. Acad. Sci. USA 90 (24): 11900–11904. doi:10.1073/pnas.90.24.11900. PMC 48092. PMID 8265645.
  26. ↑ McFadden, D.; Loehlin, J.C.; Pasanen, E.G. (1996). "Additional findings on heritability and prenatal masculinization of cochlear mechanisms: click-evoked otoacoustic emissions". Hear. Res. 97 (1–2): 102–119. doi:10.1016/0378-5955(96)00065-2. PMID 8844191.
  27. ↑ Galsworthy, M.J.; Dionne, G.; Dale, P.S.; Plomin, R. (2000). "Sex differences in early verbal and non-verbal cognitive development". Dev. Sci. 3 (2): 206–215. doi:10.1111/1467-7687.00114.
  28. ↑ Van Hulle, C.A.; Goldsmith, H.H.; Lemery, K.S. (2004). "Genetic, environmental, and gender effects on individual differences in toddler expressive language". J. Speech Lang. Hear. Res. 47 (4): 904–912. doi:10.1044/1092-4388(2004/067). PMID 15324294.
  29. ↑ Heil, M.; Kavsek, M.; Rolke, B.; Beste, C.; Jansen, P. (2011). "Mental rotation in female fraternal twins: Evidence for intra-uterine hormone transfer?". Biological Psychology 86 (1): 90–93. doi:10.1016/j.biopsycho.2010.11.002. PMID 21094200.
  30. ↑ Vuoksimma, E.; Kaprio, J.; Kremen, W.S.; Hokkanen, L.; Viken, R.J.; Tuulio-Henriksson, A.; Rose, R.J. (2010). "Having a male co-twin masculinizes mental rotation performance in females". Psychological Science 21 (8): 1069–1071. doi:10.1177/0956797610376075. PMID 20581340.
  31. ↑ Medland, S.E.; Loehlin, J.C.; Martin, N.C. (2008). "No effect of prenatal hormone transfer on digit ratio in a large sample of same- and opposite-sex dizygotic twins". Personality and Individual Differences 44 (5): 1225–1234. doi:10.1016/j.paid.2007.11.017.
  32. ↑ van Anders, S.M.; Vernon, P.A.; Wilbur, C.J. (2006). "Finger-length ratios show evidence of prenatal hormone-transfer between opposite-sex twins". Hormones and Behavior 49 (3): 315–319. doi:10.1016/j.yhbeh.2005.08.003. PMID 16143332.
  33. ↑ Dempsey, P.J.; Townsend, G.C.; Richards, L.C. (1999). "Increased tooth crown size in females with twin brothers: evidence for hormonal diffusion between human twins in utero". American Journal of Human Biology 11 (5): 577–586. doi:10.1002/(SICI)1520-6300(199909/10)11:5<577::AID-AJHB1>3.0.CO;2-Y. PMID 11533976.
  34. ↑ Elkadi, S.; Nicholls, M.E.R.; Clode, D. (1999). "Handedness in opposite and same-sex dizygotic twins: testing the testosterone transfer hypothesis". NeuroReport 10 (2): 333–336. doi:10.1097/00001756-199902050-00023. PMID 10203331.
  35. ↑ Medland, S.E.; Duffy, D.L., Wright, M.J., Geffen, G.M., Hay, D.A., Levy, F., Van-Beijsterveldt, C.E.M., Willemsen, G., Townsend, G.C., White, V., Hewitt, A.W., Mackey, D.A., Bailey, J.M., Slutske, W.S., Nyholt, D.R., Treloar, S.A., Martin, N.G., Boomsma, D.I. (2009). "Genetic influences on handedness: data from 25,732 Australian and Ditch twin families". Neuropsychologia 47 (2): 330–337. doi:10.1016/j.neuropsychologia.2008.09.005. PMC 2755095. PMID 18824185. Cite uses deprecated parameter |coauthors= (help)
  36. ↑ Vuoksimaa, E.; Eriksson, C.J.P.; Pulkkinen, L.; Rose, R.J.; Kaprio, J. (2010). "Decreased prevalence of left-handedness among females with male co-twins: evidence suggesting prenatal testosterone transfer in humans?". Psychoneuroendocrinology 35 (10): 1462–1472. doi:10.1016/j.psyneuen.2010.04.013. PMC 2950868. PMID 20570052.
  37. ↑ Cohen-Bendahan, C.C.C.; Buitelaar, J.K., van Goozen, S.H.M., Cohen-Kettenis, P.T. (2004). "Prenatal exposure to testosterone and functional cerebral lateralization: a study in same-sex and opposite-sex twin girls". Psychoneuroendocrinology 29 (7): 911–916. doi:10.1016/j.psyneuen.2003.07.001. PMID 15177706. Cite uses deprecated parameter |coauthors= (help)
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