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Prenatal testosterone transfer

Hormone transfer in the womb

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, though some studies have found that testosterone transfer can cause an exaggerated masculinization in males. There is strong evidence supporting the occurrence of prenatal testosterone transfer in rodents and other litter-bearing species, 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.

Mechanisms of transfer

Testosterone is a steroid hormone; therefore it has the ability to diffuse through the amniotic fluid between fetuses.

Consequences of testosterone transfer

During prenatal development, testosterone exposure is directly responsible for masculinizing the genitals and brain structures. This exposure leads to an increase in male-typical behavior.

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.

Mice

In mice, prenatal testosterone transfer causes higher blood concentrations of testosterone in 2M females when compared to 1M or 0M females. 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.

0M Female Mice	2M Female Mice	Physiology	Morphology	Behavior
last=vom Saal	first=F.S.	author2=Bronson, F.H.	title=In utero proximity of female mouse fetuses to males: effects on reproductive performance during later life	journal=Biol. Reprod.	year=1978	volume=19	issue=4	pages=842–853	pmid=743525	doi=10.1095/biolreprod19.4.842	doi-access=free}}	Higher fetal testosterone levels
	Earlier vaginal opening	last=vom Saal	first=F.S.	title=The production of and sensitivity to cues that delay puberty and prolong subsequent oestrous cycles in female mice are influenced by prior intrauterine position	journal=J. Reprod. Fertil.	year=1989	volume=86	pages=457–471	doi=10.1530/jrf.0.0860457	pmid=2760875	issue=2	doi-access=free}}
	last=Vandenbergh	first=J.G.	author2=Huggett, C.L.	title=The anogenital distance index, a predictor of the intrauterine position effects on reproduction in female house mice	journal=Lab. Anim. Sci.	year=1995	volume=45	pages=567–573	pmid=8569159	issue=5}}	More male offspring
	Mate and impregnated earlier	Mate and impregnated later
	vauthors=Gandelman R, vom Saal FS, Reinisch JM	title=Contiguity to male fetuses affects morphology and behaviour of female mice	journal=Nature	year=1977	volume=266	pages=722–724	doi=10.1038/266722a0	pmid=559940	issue=5604	bibcode=1977Natur.266..722G	s2cid=4150169}}	More sensitive to testosterone
Shorter anogenital distance	Longer anogenital distance
Less likely to mount other females	More likely to mount other females
	Less aggressive	More aggressive

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, while those testing perception and cognition are typically more consistent. 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

Sensation seeking
Temperament
Aggression
Toy preference

Tests of Perception and Cognition

Auditory system functioning: assessing otoacoustic emissions
Expressive vocabulary
Visio-spatial cognition: assessing mental rotation ability

Tests of Physiology and Morphology

2nd to 4th digit ratio
Tooth size
Handedness
Lateralization of language function: assessment on a dichotic listening test

References

Ryan, B.C.. (2002). "Intrauterine position effects". Neuroscience & Biobehavioral Reviews.
Clark, M.M.. (1992). "Stud males and dud males: intrauterine position effects on the reproductive success of male gerbils". Animal Behaviour.
(1990). "Intrauterine position effects in male and female swine: Subsequent survivability, growth rate, morphology, and semen characteristics". Journal of Animal Science.
(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.
Tapp, A.L.. (2011). "Evaluating the twin testosterone transfer hypothesis: A review of the empirical evidence". Hormones and Behavior.
Gorodeski, G.I.. (1995). "Sex hormone modulation of flow velocity in the parametrial artery of the pregnant rat". Am. J. Physiol..
Nelson, R.J.. (2000). "An Introduction to Behavioral Endocrinology, 2nd ed.". Sinauer Associates.
Breedlove, S.M.. (1994). "Sexual differentiation of the human nervous system". Annu. Rev. Psychol..
Goy, R.W.. (1972). "The effects of testosterone propionate administered before birth on the development of behaviour in genetic female rhesus monkeys". UCLA Forum Med. Sci..
vom Saal, F.S.. (1990). "Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions". Biol. Reprod..
vom Saal, F.S.. (1978). "In utero proximity of female mouse fetuses to males: effects on reproductive performance during later life". Biol. Reprod..
McDermott, N.J.. (1978). "Contiguity to male fetuses influences ano-genital distance and time of vaginal opening in mice". Physiol. Behav..
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..
Vandenbergh, J.G.. (1995). "The anogenital distance index, a predictor of the intrauterine position effects on reproduction in female house mice". Lab. Anim. Sci..
(1977). "Contiguity to male fetuses affects morphology and behaviour of female mice". Nature.
vom Saal, F.S.. (1983). "High fetal estrogen concentrations: correlation with increased adult sexual activity and decreased aggression in male mice". Science.
Quadagno, D.M.. (1987). "The effects of intrauterine position on competition and behavior in the mouse". Physiol. Behav..
(1984). "Fetal effects on sexual behavior and aggression in young and old female mice treated with estrogen and testosterone". Hormones and Behavior.
(2005b). "Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings". Neuroscience and Biobehavioral Reviews.
Resnick, S.M.. (1993). "Sensation seeking in opposite-sex twins: an effect of prenatal hormones?". Behavior Genetics.
Rodgers, C.S.. (1998). "Gender-typed toy play in dizygotic twin pairs: a test of hormone transfer theory". Sex Roles.
McFadden, D.. (1993). "A masculinising effect on the auditory systems of human females having male co-twins". Proc. Natl. Acad. Sci. USA.
McFadden, D.. (1996). "Additional findings on heritability and prenatal masculinization of cochlear mechanisms: click-evoked otoacoustic emissions". Hear. Res..
Galsworthy, M.J.. (2000). "Sex differences in early verbal and non-verbal cognitive development". Dev. Sci..
Van Hulle, C.A.. (2004). "Genetic, environmental, and gender effects on individual differences in toddler expressive language". J. Speech Lang. Hear. Res..
Heil, M.. (2011). "Mental rotation in female fraternal twins: Evidence for intra-uterine hormone transfer?". Biological Psychology.
Vuoksimma, E.. (2010). "Having a male co-twin masculinizes mental rotation performance in females". Psychological Science.
Medland, S.E.. (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.
van Anders, S.M.. (2006). "Finger-length ratios show evidence of prenatal hormone-transfer between opposite-sex twins". Hormones and Behavior.
Dempsey, P.J.. (1999). "Increased tooth crown size in females with twin brothers: evidence for hormonal diffusion between human twins in utero". American Journal of Human Biology.
Elkadi, S.. (1999). "Handedness in opposite and same-sex dizygotic twins: testing the testosterone transfer hypothesis". NeuroReport.
(2009). "Genetic influences on handedness: data from 25,732 Australian and Ditch twin families". Neuropsychologia.
Vuoksimaa, E.. (2010). "Decreased prevalence of left-handedness among females with male co-twins: evidence suggesting prenatal testosterone transfer in humans?". Psychoneuroendocrinology.
(2004). "Prenatal exposure to testosterone and functional cerebral lateralization: a study in same-sex and opposite-sex twin girls". Psychoneuroendocrinology.

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