Prenatal Influences on Human Sexual Orientation

Arch Sex Behav (2017) 46:1583–1592 DOI 10.1007/s10508-016-0904-2 TARGET ARTICLE Prenatal Influences on Human Sexual Orientation: Expectations versus Data S. Marc Breedlove1 Received: 17 June 2016 / Revised: 10 November 2016 / Accepted: 13 November 2016 / Published online: 7 February 2017 Ó Springer Science+Business Media New York 2017 Abstract Innon-humanvertebratespecies,sexualdifferentiation dence of greater prenatal androgen exposure than groups of straight of the brain is primarily driven by androgens such as testosterone women, while groups of gay men have, on average, a greater propor- organizingthebrainsofmalesinamasculinefashionearlyinlife, tion of brothers among their older siblings than do straight men. while the lower levels of androgen in developing females orga- nize their brains in a feminine fashion. These principles may be Keywords Sexual orientation Á Testosterone Á Androgens Á relevanttothedevelopmentof sexual orientationinhumans, Birth order Á Digit ratios Á Otoacoustic emissions 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 Introduction werestraightwomen.Thus,theevengreaterlevelsofprenatalandro- gen exposure experienced by fetal males may explain why the vast Mostofus havewondered aboutthe extenttowhich ourbehavior majority of them grow up to be attracted to women. However, the is a function of socialization, culture, and the learning process same markers indicate no significant differences between gay and while growing up, and the extent to which our behavior can be straight men in terms of average prenatal androgen exposure, so the attributed to more basic processes, what might be regarded as varianceinorientation in mencannotbeaccounted forbyvariance in ‘‘biological’’influences. Often this is posed as the relative con- prenatal androgen exposure, but may be due to variance in response tributions of nature versus nurture, or genetic versus environmen- to prenatal androgens. These data contradict several popular notions tal influences. But even a superficial understanding of the nature- about human sexual orientation. Sexual orientation in women is said nurture‘‘debate,’’or of environmental regulation of gene expres- to be fluid, sometimes implying that only social influences in adult- sion, reveals these distinctions to be very difficult to sort out when hood are at work, yet the data indicate prenatal influences matter as you consider the details. So instead of those amorphous, difficult- well. Gay men are widely perceived as under-masculinized, yet the to-define distinctions, it may be more productive to weigh the data indicate they are exposed to as much prenatal androgen as relative contributions of a more precisely defined duality, namely straight men. There is growing sentiment to reject‘‘binary’’concep- prenatalversuspostnatalinfluences.Theonethingwecansaywith tions of human sexual orientations, to emphasize instead a spectrum some confidence is that prenatal influences cannot be attributed to of orientations. Yet the data indicate that human sexual orientation is social interactions, as the fetus is insulated from awareness of the sufficiently polarized that groups of lesbians, on average, show evi- behavior of any individuals (other than the mother, and her ave- nues of social influence, her voice perhaps, are relatively limited). If events before birth influence the individual’s later behavior, at least we can say they could not have been initiated by the indi- & S. Marc Breedlove viduallearningaboutbehaviorfromothers.Ofcourse,totheextent [email protected] prenatal events alter the individual’s future behavior, that altered behavior may affect the way other people respond to the indi- 1 Neuroscience Program and Departments of Psychology, vidual. From thence we spiral down the rabbit hole of iterative Integrative Biology, Michigan State University, 293 Farm Lane, Giltner Hall Room 108, East Lansing, MI 48824-1110, rounds of environmental influences on gene expression, which USA affects later experiences, which influences future gene expression 123 1584 Arch Sex Behav (2017) 46:1583–1592 and so on, indefinitely. What can we say about the relatively sim- other monkeys (Goy & Phoenix, 1972). Thus, for me, the ques- pler question of prenatal versus postnatal influences on human tion remained whether the organizational hypothesis also holds behavior, specifically on sexual orientation? true for the human brain and for sex differences in human behavior. Clearly there are influences other than prenatal andro- gensonhumanbrainsexualdifferentiation—evenrecenthistory Weighing Social Influences versus Prenatal makes that obvious. The big question is whether there is any Influences residual influence of prenatal gonadal steroids on human behavior at all. Having spent most of my adult life investigating sex differences To make this personal, while in graduate school and as a inbehaviorinnon-humananimals,Ihavewonderedwhetherthe young professor, I happily studied the influence of early hor- resultsof animal studies haveany relevance to sex differences in moneexposureonthemasculinizationofthenervoussystemin human behavior. We know that some sex differences in human non-human animals. There it was quite clear that I could make behavior wax and wane over history and clearly are modified by various parts the brain or spinal cord as masculine or feminine culture. Some sex differences in mathematical performance, for as I wanted simply by controlling how much testosterone the example, have been steadily decreasing just in my lifetime, so organism was exposed to. When the rat was exposed to andro- thatnowtherearesome societieswheregirlsperform betterthan gen early in life, then the brain would be organized in a mas- boys, on average, in tests of math ability (Guiso, Monte, Sapien- culinefashion.Iftheindividualwasnotexposedtotestosterone za, & Zingales, 2008). Still, there are other sex differences in early in life, then the brain would be organized in a feminine human behavior that persist, at least for now. So it is fair to ask fashion. Eventually we found some brain regions that were sex- whether they are caused by the same sorts of prenatal events that ually dimorphic not due to perinatalandrogens, but were respond- leadto sexdifferencesin animalbehavior,whicharewellunder- ing to androgens in adulthood (Cooke, Tabibnia, & Breedlove, stood. 1999), butstillhormonesseemedtoaccountentirely forthesexdif- For over 50 years now, a relativelysimple andpowerful expla- ference.Behavioralcorrelatesof thesexdifferencesinthe structure nation of how sex differences in behavior arise in mammals— of the brain were harder to demonstrate but, when found, were that sex differences in the brain are created through the same always consistent with brain changes (e.g., Cooke, Chowanadisai, prenatal events that bring about sex differences in the body—has &Breedlove,2000;DeJongeetal.,1989; Gurney, 1982). Of dominated the literature. Just as androgenic hormones like testos- course, as I published these studies and sought funds to pay for terone work early in life to form a male phenotype of the body, so them,Ialwaysindicatedthattheseprocessesmightapplytohuman too, do those hormones masculinize the developing brain to mas- behavior. But in my private thoughts, I was very skeptical of the culinize behavior in animals. And just as the relative absence of idea. Long after I was a Full Professor of Psychology, I had serious androgens early in life causes the body to develop a feminine doubts about whether androgens working early in life have any phenotype, so too will the absence of early androgens result in the influence whatsoever on the developing human brain. development of a feminine nervous system. From this perspec- There were several reasons for that skepticism. Once people tive, the brain is just one more part of the body poised to detect a started finding sex differences in brain structures in humans that single, unifying signal: if androgens are high during a sensitive werehomologoustothosefoundinanimals,adistinctionbecame period, various cells and tissues distributed throughout the body obvious. The extent of sexual dimorphism in these brain regions should form a male phenotype, while if androgens are low they was much smaller in humans than in other animals. For example, should form a female phenotype. There is a pleasing simplicity to the SDNPOA is 5–6 times larger in volume in male rats than the idea that a solitary signal, androgen, coordinates the feminine females (Gorski, Harlan, Jacobson, Shryne, & Southam, 1980). or masculine development of every part of the body, so that indi- Yet in humans, depending on which hypothalamic nucleus you viduals that are going to reproduce as females have both the believe is homologous to the rat SDNPOA, you see at most a genitalia and behaviors to be successful in that role, and so do twofolddifferencebetweenmenandwomen(LeVay,1991;Swaab those that are going to reproduce as males. &Fliers,1985), and less than a threefold sex difference in rhesus That relatively simple but powerful organizational hypoth- monkeys (Byne, 1998). Likewise, the brain regions that control esis (Phoenix, Goy, Gerall, & Young, 1959) has been applied to song are 5–6 times larger in males, who sing, than in females, who hundredsofpublishedstudiesofanimalsandcanaccountforthe typically do not (Nottebohm & Arnold, 1976). We just never see vastmajorityof sexdifferencesnotonlyin behavior,butin brain sexual

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