Prenatal hormones play only a minor role in making anyone gay, straight or transgender
This comment is longer than usual, because the subject matter is unusually significant.
A recent swathe of research on the effects of exposure to testosterone in the womb shows that its influence on human sexual orientation is weak to modest. Rather than the overwhelming influence on sexual orientation the researchers had been expecting to find it is only between 16-27%. This finding is for heterosexuality, and the influence on homosexuality and transgender should be even less. (A corroborating research paper is in preparation.) Basically, one is not born straight, gay or transgender.
Phoenix et al. published a paper in 1959 on the development of sexuality, i.e. sexual attraction (Phoenix et al. 1959). It has had more than 950 citations. Based on guinea-pig experiments, the authors argued that the well-known prenatal testosterone surge in mammals - including humans - organised the brain to be male, but that this organisation was essentially dormant until puberty when pubertal sex hormone surges activated it and sexual attraction occurred. The thinking was that this “male” brain could not be changed by the hormone surges of puberty but that pubertal surges flicked a switch that simply revealed it and kick-started sexual attraction according to the prenatally pre-determined sexual orientation. The theory also held that social interactions, e.g., with parents after birth, also had no role in male brain organisation. It became known as the organisational-activational hypothesis.
At the time the hypothesis was an explanation for OSA (opposite-sex attraction). Later it was used as an explanation for SSA (same-sex attraction) based on the theory that for males the testosterone surge was perhaps weaker than usual, and perhaps for females there was some stronger than usual testosterone exposure from a hypothetical and unknown source. (Female foetuses are also exposed to small amounts of testosterone in the normal course of pregnancy.) The same idea is commonly invoked today for the origin of transgender feelings. In all cases advocates of the theory imply that the influence of prenatal testosterone is very large, and probably overwhelming.
Both parts of the hypothesis were difficult to test in humans. To do so researchers needed to devise a way to detect both prenatal hormonal surges before birth and sexually dimorphic brain organisation after birth. Tools to do this became widely available about a decade ago and results confirm prenatal testosterone is involved in forming brain structure. But this posting makes the point that the effects are much weaker than expected.
This posting, will mainly survey the influence of prenatal testosterone on brain anatomy. The effects of gene expression on “brain gender” will be discussed in a later posting.
Fetal testosterone can now be measured. Researchers can take advantage of a procedure called amniocentesis in which samples of amniotic fluid are withdrawn from pregnant women for genetic testing. With consent, they have analysed these for testosterone to determine the nature of the pre-natal testosterone surge, and subsequently applied a battery of tests to these children from birth to 11 years to see if there is a correlation between testosterone exposure and gendered behaviour. There was some Dutch research, but much of the research has been done in an autism research unit at the University of Cambridge and the chief researcher was the well-known Simon Baron-Cohen.
In a series of papers over a decade, he and others, have shown correlations of fetal testosterone with many male-related traits. These were with: autism (Auyeung et al. 2009a; Auyeung et al. 2010), inversely with empathy (Chapman et al. 2006), positively with male-type child play (Auyeung et al. 2009b) (though (Knickmeyer et al. 2005), (van de Beek et al. 2009) found no correlation), inversely with degree of eye contact (Lutchmaya, Baron-Cohen, and Raggatt 2002a), negatively with greater vocabulary (Lutchmaya, Baron-Cohen, and Raggatt 2002b), positively with the 2Digit/4Digit finger length ratio (Lutchmaya et al. 2004) positively with some visuospatial ability but not mental rotation (Auyeung et al. 2011), positively with hand strength (Lust et al. 2011) and positively with brain lateralisation, and male-type brain grey-matter features using MRI scans (Lombardo et al. 2012), (Chura et al. 2010), (Mercure et al. 2009). Some of these tests were done on 8-11 year children, a long time after the fetal testosterone measurements. Any results directly on sexual attraction have not thus far been published.
These features were tested because they were believed to differ in males and females. They were the best ones to test in childhood for gender traits, but there was a large overlap in results between male and female. Of particular interest are the papers which try to link fetal testosterone with sexually dimorphic anatomical structures, particularly finger length ratios and brain structure (Lombardo et al. 2012). The strength of the association is almost identical for these two. Correlation coefficients range from 0.45 to 0.49 (maximum 1.0 for perfect correlation), a statistically real effect. To find the degree of influence, or fraction of variance explained, one squares that correlation coefficient, and in summary 16-27% of the total variance (roughly total influences) on finger length and brain structure was explained; 73-84% is left unexplained. This makes the fetal testosterone influence weak to modest at best. The authors do not consider that, or other possible implications.
The maximum correlations were used for the above calculation. The other correlations between fetal testosterone and later male traits were much weaker or non-existent. Those who have followed similar studies over the last few decades will be hesitant to accept any brain structure results until replicated, because there have been numerous papers studying brain sexual dimorphism which have failed the usual replication test.
Another major caveat is that the brain scans were done well after the six month post-birth testosterone surge which was not measured by Simon Baron-Cohen. The fetal testosterone association could ultimately be found to be weaker in its effects than the post-birth association. It is also a general principle that the greater the age gap between two events in the history of an individual (e.g. fetal testosterone exposure and adolescent attraction) the less the influence and the weaker the correlation between the two.
Neither is the hypothesis being tested in its purest form. Its proponents believe that sexual attraction will only reveal itself at puberty in an already prenatally organised “male “ brain, so the brain structure of these children should be examined again at puberty to determine whether structural changes have occurred in the brain at that time - and it is likely that will be done. However, although a puberty test would be more explicit, an influential stream of thought is now that first sexual attraction to either the opposite sex or same sex occurs before puberty, at an average of 10 years, but with a wide age range (Herdt et al. 2000). This age range has been covered by the work of Baron-Cohen and Lombardo and, although it was not discussed , the results should say something significant about any correlation between fetal testosterone, increasing brain dimorphism and first sexual attraction.
The paper by Lombardo et al. is particularly important in this regard because it is explicitly put forward as a test of the Phoenix et al. hypothesis for the brain – the idea that the “male brain”is fully organised prenatally. The researchers were expecting to find an overwhelmingly strong correlation but the association was surprisingly weak. This has important implications: although most research finds there is a correlation between fetal testosterone and later maleness, it does not dictate traits associated with male OSA, but only modestly influences the brain anatomy.
A result of this modest strength is similarly found when one investigates the wide spread of ages in first OSA attraction rather than puberty itself. The wider the age spread in the appearance of any trait the less likely it is to be genetic, or biologically programmed. A similar rather modest result is found when one tries to derive a genetic influence on OSA using twin studies, as given in the research report of (Hershberger 1997). The genetic or prenatal effect on OSA is modest. One is not destined to become OSA . Like virtually every trait studied, OSA seems to be multifactorial; there are many influences. It should be noted that this is an important result for those who believe, following Phoenix et al, that one is born heterosexual; or rather born to be heterosexual, and no nurture input is needed. Contrary to that belief, sexual orientation is not destined; if it were the correlation between fetal testosterone and later brain structure would be 1.0 (100%).
What does this modest effect mean for homosexual and transgender attraction?
There is an implication in all this for the development of SSA (same sex attraction). If supporters of the organisational-activational hypothesis are going to argue that sexual orientation is influenced by fetal testosterone, even though this was not directly examined in the Lombardo et al. paper, SSA should be no more influenced by prenatal hormones than OSA, so that the effect should be weak to modest, not dominant – as proponents of this line like to claim. The same applies to the development of transgender.
Research has increasingly revealed many processes at work in the development of sexual orientation/attraction including non-hormonal. E.g., since the time of the Phoenix et al. paper, researchers have discovered that there are some prenatal sexually dimorphic effects in the brain dependent directly on the sex chromosomes, even where there is no influence of sex hormones (and even no gonads).
Further, since maternal care significantly influences future sexual orientation (at least in rats) it is the opinion of most researchers that there are multiple influences at work rather than merely the prenatal testosterone surge.
This leads to a contemporary comment on the Phoenix paper “… our current knowledge of sex-based neurobiology has outgrown this simplistic model. Multiple lines of research have contributed to this conclusion” (Reinius 2011) p15).
The contribution of prenatal sex hormones to OSA or SSA is not 100% as many have believed but is about 25%; a minor contribution. In that sense one is not born gay or straight or transgender.
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