© Simon LeVay, 2003. Latest update: April 2009

 

This page is an overview of theories and research on the topic of sexual orientation, with emphasis on biological studies. I welcome corrections, comments, and suggestions for other studies that should be covered (email me) (return to home page).

 

Non-biological theories

Psychoanalytic theories

Early in the 20^th century, Sigmund Freud postulated that family dynamics influence a child’s ultimate sexual orientation. For example, a dominant, close-binding mother, or an absent or distant father, might steer a boy toward homosexuality by disrupting his exit from the postulated “Oedipal phase” of psychosexual development (Freud 1957). Girls might become lesbian because of unconscious hatred of their mothers, envy of a brother’s penis, and the like (Freud 1920/1955). Retrospective studies confirm that gay men tend to describe their relationships with their mothers as unusually close and with their fathers as distant or hostile (Bell, Weinberg et al. 1981; Freund and Blanchard 1983).

Comment: These retrospective findings don’t necessarily mean that parental attitudes influence the child’s sexual orientation in the way Freud envisaged, however. A contemporary American analyst has suggested that parental attitudes to pre-gay children, such as a father’s withdrawal or hostility, may actually be a response to gender-variant traits in the child rather than a cause of them (Isay 1989; Isay 1996).

Behaviorism/socialization

Learning theorists have suggested that gendered traits, including sexual orientation, emerge from a conscious or unconscious “training regimen” imposed by parents, teachers, peers, and society in general (Money and Ehrhardt 1971). Most feminist thinkers have also attributed the development of gendered traits to socialization.

Comment: The main difficulty with these ideas is that heterosexual parents don’t seem to inculcate homosexuality or gender-nonconformity, in fact they often attempt to prevent these traits in children who nevertheless become gay. Parents who happen to be gay themselves might tolerate or even foster gender variance and homosexuality in their children, but in fact the children of gay parents usually become heterosexual (Stacey and Biblarz 2001). One much-publicized attempt to change a child’s gender and future sexual orientation by parental socialization (after his penis was accidentally destroyed during circumcision) ended in failure (Colapinto 2000).

Effect of sexual experiences

It has been proposed that early sexual experiences (pleasant or traumatic) influence sexual orientation—that a girl who is raped by a man at an early age may be “turned off” men and thus become lesbian, for example, while a boy who is seduced by a man (or molested by an older brother) and who derives sexual pleasure from the experience may become gay (Churchill 1967; Cameron and Cameron 1995).

Comment: Such ideas fail to explain how it is that many people whose initial sexual experiences are heterosexual and consensual nevertheless become gay, or how it is that children who attend single-sex boarding schools, where consensual homosexual encounters are common, are no more likely to become homosexual adults that are children who do not attend such schools (Wellings, Field et al. 1994).

Social constructionism

This school of thought proposes that a person’s identity as gay, straight, or bisexual is a label imposed by society and internalized by the individual, rather than arising from within (Foucault 1978; Halperin 1990).

     Comment: Social constructionism has contributed valuable insights to our understanding of human sexuality in its cultural context, but it has had relatively little to say about the question that interests us here, which is why specific individuals become gay, straight, or bisexual.

Biological theories

General comments

A contrasting view is that sexual orientation is determined or influenced by biological factors such as genes and hormones. Of course, there doesn’t have to be a sharp distinction between biological and life-experience theories. It’s conceivable, for example, that a close-binding mother might induce hormonal changes in the young child that in turn lead to adult homosexuality. Conversely, a biological trait such as facial beauty might influence parents to treat a son in such a way as to steer him toward homosexuality. At the very least, though, testing biological and life-experience theories require the application of very different techniques and thus tend to engage researchers with different training and backgrounds.

 

Biological theories of sexual orientation have a long history. Magnus Hirschfeld, the German sexologist and gay-rights pioneer, promoted such theories early in the 20^th century. Still, Freudian, behaviorist, and social-constructionist thinking dominated thinking on the topic for most of the century. Only in the 1980s and 1990s did biological ideas re-emerge in a significant way. This re-emergence paralleled a remarkable increase in tolerance and acceptance of gay people in many Western societies. It seems likely that these parallel trends reflected a two-way interaction: increasing acceptance of (and familiarity with) gays fostered a belief in biological theories, and vice versa.

 

Sexual orientation is a gendered trait: most men are sexually attracted to women more than they are to men, and most women are sexually attracted to men more than they are to women. Homosexual people are sex-atypical, at least with respect to their sexual orientation. Biological theories of sexual orientation commonly, though not always, include the idea that sexual orientation is embedded within a larger constellation of gendered traits, and that biological factors influence multiple gendered traits simultaneously. Whatever ultimate biological factors influence a person to become homosexual, these factors may promote the development of other characteristics—anatomical, physiological, molecular-genetic, or psychological—that are sex-atypical. Given that the ultimate factors may not be directly detectable (if they operated during fetal life, for example), the presence of other sex-atypical traits in gay people may be taken as an indicator that those undetectable factors were in fact at work. Still, the presence of sex-atypical traits in gay people doesn’t always compel a biological interpretation—it might be that certain life experiences promote both homosexuality and other sex-atypical characteristics.

 

To give a concrete example: it’s been well documented that gay people, on average, display some sex-atypical psychological characteristics during childhood (Bailey and Zucker 1995). Gay men, for example, tend to report that they had less interest in rough-and-tumble sports than other boys. A prospective study showed that boys who are very strongly gender-nonconformist have a high likelihood of developing into gay or bisexual adults (Green 1987). But this connection between childhood gender-nonconformity and adult homosexuality could arise for genetic reasons (genes promoting a spectrum of gender-nonconformist traits including homosexuality) or for environmental reasons (e.g., parental encouragement these same traits). It’s also possible that genes cause childhood gender-nonconformity and that environmental factors (e.g. the hostile reactions of peers) cause gender-nonconformist children to become gay. Thus the fact that there is a correlation between homosexuality and some other trait doesn’t in itself distinguish between different possible causes.

Genes

Animal studies.

In the fruit fly, Drosophila, sexual orientation appears to be under the control of a single gene named fruitless (“fru”) (Demir and Dickson 2005). fru is alternatively spliced (read off into messenger RNAs and proteins in a different fashion) in males and females. If a female fruit fly is engineered to splice fru in the male-specific fashion, she will approach and court other females and attempt to copulate with them. If a male fruit fly is engineered to splice fru in the female-specific fashion, he will fail to approach or court females. A chain of neurons in the male fly’s nervous system expresses fru and splices it in the male-specific fashion (Stockinger, Kvitsiani et al. 2005). These neurons include olfactory receptors that are probably involved in the detection of female sex pheromones, as well as other neurons that are synaptically connected with these olfactory neurons and with each other. There are no obvious anatomical differences between these neurons in male and female flies: thus, they probably differ in some physiological or chemical attribute that causes them to generate (in males) the male-specific sexual behavior.

    Comment: In insects, sex differentiation is cell-autonomous, so neurons are caused to splice fru in male-specific or female-specific fashion by the sex-determining genes in those same cells. Thus homosexuality (a dissociation between anatomical sex and sex-typical sexual orientation) is unlikely to occur, and in fact has not been observed outside of molecular-genetics labs. The situation in humans is different in that sexual differentiation is not cell-autonomous but depends in large part on circulating sex hormones. This may allow for greater variability in sexual orientation, whether we are talking about genetic or non-genetic causes.

 

Sibling studies. Most of the evidence for a genetic influence on human sexual orientation comes from family and twin studies. Homosexuality clusters in particular families, especially among siblings. Thus, the brothers of gay men are reported to have about a 22 percent chance of themselves being gay, whereas the brothers of heterosexual men have only about a 4 percent chance of being gay (Pillard and Weinrich 1986). Similarly, the sisters of lesbians have an increased chance of being lesbian (Bailey and Benishay 1993). This clustering in largely sex-specific: the existence of a lesbian in a family has little effect on the chances that her brothers will be gay, or vice versa.

  Comment: Family clustering is consistent with a genetic influence, but it does not by itself distinguish between genetic and environmental causes. For example, a mother who treats one son in such a way as to make him gay might well do the same with another son. To the extent that the clustering does have a genetic cause, the sex-specificity of the clustering would imply that different genes contribute to male and female homosexuality. This is hardly surprising since they are really different phenomena: male homosexuality is sexual attraction to males and female homosexuality is sexual attraction to females.

 

Twin studies. Most twin studies have focused on the concordance rate for homosexuality. This is the likelihood that, if one twin is gay, his or her co-twin will be gay too. If genes influence sexual orientation, the concordance rate should be higher for twin pairs who are monozygotic (“identical”) than for twin pairs who are dizygotic (“fraternal”). That’s because monozygotic twins share all the same genes, whereas dizygotic twins share only about half their genes. If genes absolutely determined sexual orientation the concordance rate for monozygotic twins should be 100%.

             One early study did report a near-100% concordance rate for male monozygotic twins (Kallmann 1952). More recent studies have come up with much lower figures, but have generally reported higher concordance rates for monozygotic than for dizygotic twins, consistent with a genetic influence on sexual orientation. In one study the concordance rate was 52% for male monozygotic twins compared with 22% for male dizygotic twins (Bailey and Pillard 1995). A comparable study of female twins came up with concordances of 48% and 16% respectively (Bailey, Pillard et al. 1993).

Although these studies suggest that there is a substantial influence of genes on sexual orientation in both men and women, there are problems of interpretation. For one thing, it is difficult to get from the concordance rates to a measure of heritability (meaning, simply put, the fraction of the total causation of homosexuality that is genetic). If it is the case that monozygotic twins experience a more similar environment than do dizygotic twins (being treated more similarly by their parents, for example), and these environmental factors influence sexual orientation, then the concordance rate would be higher for monozygotic twins for that reason alone. There is in fact no reason to think that this scenario is the case, but it is a theoretical possibility.

Another problem has to do with ascertainment bias. Typically, researchers do these twin studies by advertising for individuals who are gay and have a twin, then they check on the other twin’s sexual orientation. But if the likelihood that a person responds to the ad is affected by whether his/her twin is also gay or not, this could throw off the statistics. To get away from this problem, Bailey and colleagues did one study using a pre-existing twin registry (Bailey, Dunne et al. 2000). This study came up with lower concordance rates than previous studies, especially in women. Interestingly, the researchers found that childhood gender nonconformity—a common precursor of adult homosexuality—was significantly heritable in both sexes.

           There is one small study of monozygotic twins reared apart (Eckert, Bouchard et al. 1986). Of four female pairs in which one twin was lesbian, none of the co-twins were lesbian. Of two male pairs in which one twin was gay, one of the co-twins was also gay, while the other was bisexual.

Comment: There remains considerable uncertainty about the heritability of homosexuality: it is probably significantly heritable in men but may be only slightly heritable or not heritable at all in women.

 

Candidate-gene study. One approach to the question of genes influencing sexual orientation is to pick a gene that might conceivably play a role and to compare its DNA sequence in gay and straight people. One group of researchers picked the androgen receptor gene, a gene that plays the key role in mediating testosterone’s influence on the body and brain (Macke, Hu et al. 1993). They could not find any differences between gay and straight men, however.

 

Linkage studies. A contrasting approach is to scan part or all of the genome, looking for sites where pairs of gay siblings inherit the same DNA more frequently than would be expected on a chance basis (“linkage analysis”). Dean Hamer’s group reported finding (in pairs of gay brothers) such a site on the X chromosome—in a region called Xq28 (Hamer, Hu et al. 1993). They concluded that a gene influencing male sexual orientation was probably located in this region. (The choice of the X chromosome for study was motivated by family data suggesting that gay men inherit a predisposition to homosexuality from their mothers — the X chromosome is the only chromosome that males inherit exclusively from their mothers.) Hamer’s group replicated the finding in a second sample but there has not been an independent confirmation, and in fact one group has reported failing to replicate the finding (Rice, Anderson et al. 1999). Thus the claim of a “gay gene” on the X chromosome remains unverified.

In 2005 a group led by Brian Mustanski (and including Hamer) reported on a genome-wide linkage scan (Mustanski, Dupree et al. 2005). They did not confirm the Xq28 linkage but they did find evidence for linkage at three other sites — on chromosomes 7, 8, and 10. The researchers were not able to perform a statistical analysis to evaluate whether these results were due to chance or to the actual existence of genes influencing sexual orientation at those three locations.

        Comment: Even in the case of clearly “biological” traits such type 2 diabetes, which is known to be under genetic influence, the search for the responsible genes has proven frustratingly difficult. Thus is should be no surprise that researchers have had a hard time pinning a complex trait like sexual orientation down to specific genes. It may be that a number of genes have effects that are individually weak and therefore difficult to detect, or that certain genes do have strong effects but only in certain families or under certain environmental conditions. Given the evidence that sexual orientation is indeed partly inherited, at least in men, the continued search for the responsible genes and their mechanism of action is certainly warranted.

 

Genomic imprinting. This is the phenomenon whereby some genes acquire different molecular labels depending on whether they are inherited from the mother or the father; this labeling affects gene expression and development in the offspring. An article from Dean Hamer’s lab speculates that imprinting could play a role in the development of sexual orientation (Bocklandt and Hamer 2003).

 

X-inactivation. Bocklandt and Hamer reported that women with gay sons—especially those with two gay sons—are more likely than women without gay sons to show extreme skewing of X-inactivation (that is, more than 90 percent of their cells show inactivation of the same X chromosome)(Bocklandt, Horvath et al. 2006).

           Comment: These data could be taken to strengthen Hamer’s 1993 conclusion that a gene or genes on the X chromosome influence male sexual orientation. However, the current study depends primarily on the same subject set that was used for that earlier study. Given that subsequent studies, including Mustanski’s, haven’t confirmed the linkage reported in the 1993 study, one may wonder if that subject set was atypical in some way. Thus replication of the current findings with an entirely new sample would be desirable.

 

Gay genes and evolution. The existence of genes promoting homosexuality is counter-intuitive, since such genes should reduce their owner’s reproductive success and thus, over many generations, they should be eliminated from the gene pool. A number of people have considered the various ways in which gay genes might persist (Wilson 1978; Weinrich 1987; Ruse 1988; Hamer and Copeland 1994; Ridley 1994; Bailey 2003). Here are some of the ideas that have been put forward:

1.  Gay genes might persist if gay people, though having few children themselves, promote the reproductive success of their siblings (“kin selection”).

4. A gene for sexual attraction to men would cause homosexuality in men but might cause a “hyper-heterosexuality” in women, thus increasing their reproductive success—and vice versa. The positive effect on the reproductive success of one sex might balance the negative effect in the other sex. Consistent this hypothesis, an Italian study reported that the female maternal relatives of gay men have more offspring than those of heterosexual men, as if a gene predisposing simultaneously to male homosexuality and female “hyper-heterosexuality” were being transmitted on the X chromosome (Camperio-Ciani, Corna et al. 2004).

5.  It’s possible that, through much of human evolution, people have been socially compelled to marry and have children regardless of their sexual orientation. In this case, the negative effect of a gay gene on reproductive success might be small, and might be outweighed by some other, unknown benefit conferred by the gene.

6. The elimination of gay genes from the population (by non-reproduction of gay people) might be balanced by the occurrence of new mutations. For this to be the case, the mutation rate for gay genes would have to be exceptionally high.

Comment: None of these theories are particularly persuasive. The evolutionary value of gay genes may become clearer if and when such genes are identified and their mechanism of action determined.

Hormones

Adult hormone levels.  Most studies have failed to find significant differences in the levels of circulating sex hormones between homosexual and heterosexual adults of the same sex (Meyer-Bahlburg 1984).

 

Prenatal hormones: background. In experimental animals it’s been well established that the sexual differentiation of the body and brain results primarily from the influence of sex hormones secreted by the testes or ovaries (Arnold 2002). Males have high levels of testosterone in fetal life (after functional development of the testes) and around the time of birth, as well as at and after puberty. Females have low levels of all sex hormones in fetal life, and high levels of estrogens and progestagens starting at puberty. High prenatal testosterone levels organize the brain in a male-specific fashion; low levels testosterone permits it to organize in a female-specific fashion. Hormones at puberty activate the circuits laid down in prenatal life but do not fundamentally change them. Thus, the range of sexual behaviors that adult animals can show is determined in large part by their prenatal/perinatal hormone exposure—manipulating these hormone levels can lead to atypical sex behavior or preference for same-sex sex partners as well as a range of other gender-atypical characteristics.

Nevertheless, prenatal/perinatal hormones may not be the entire story. Changes in adult hormone levels can change brain anatomy in some cases (Cooke, Tabibnia et al. 1999). Furthermore, some aspects of the prenatal sexual differentiation of the brain seem to be independent of sex hormones and probably reflect the direct effects of the brain’s chromosomal sex on its own development (Arnold 2003). Whether these direct effects are significant for the development of any gendered traits in humans is unknown.

Based on this animal research a number of scientists, especially the German neuroendocrinologist Günter Dörner, have promoted a prenatal hormonal theory of homosexuality (Dörner 1969). This theory postulated that in human fetuses destined to become homosexual adults, the sexual differentiation of the brain proceeds in a sex-atypical direction. The cause could be atypical levels of sex hormones (e.g., unusually low levels of testosterone in the case of a male fetus, or unusually high levels in a female fetus) or some difference in the way the brain responds to hormones, such as a genetic peculiarity of the androgen receptor (see above).

Dörner initially presented his theory as part of a pathological conception of homosexuality and even as a tool for preventing it through medical means. This did not endear him to the gay community. There is no intrinsic reason why his theory should be seen as less gay-friendly than other theories, however (LeVay 1996). Although the prenatal hormonal theory has not been proved or disproved in the decades since Dörner proposed it, a body of supportive evidence has accumulated, and it is probably the dominant idea among those who think about sexual orientation from a biological perspective.

Attributing sexual orientation to prenatal hormone levels is not an ultimate explanation, because the question remains as to how those levels (or the brain’s response to them) come to be different in pre-gay and pre-straight fetuses. At one extreme, the reason for these differences might be genetic, as with the androgen receptor hypothesis mentioned above or the case of congenital adrenal hyperplasia, discussed below. At the other extreme the reason might be environmental, as with Dörner’s maternal stress theory, discussed below. It’s also possible that essentially random developmental processes could be responsible. In species such as rats where the mother carries multiple fetuses simultaneously, a female fetus that happens to be located next to a male fetus can absorb testosterone from its neighbor, resulting in some masculinization of her sexual behavior in adulthood (Clemens, Gladue et al. 1978; Meisel and Ward 1981). Since the sex of a fetus’s neighbor is random, the ultimate cause of the masculinized behavior is also random. There are probably countless such random processes occurring prenatally, even in fetuses who are singletons. (Human females who had a male twin are not thought to be especially likely to be lesbian. Some studies have reported other gender-atypical traits in these women (McFadden 1993), but negative findings have also been reported (Henderson and Berenbaum 1997)).

 

Congenital adrenal hyperplasia (CAH). This condition is caused by a genetic defect in one of the enzymes that are involved in the synthesis of corticosteroid hormones. It is marked by excessive levels of androgens (testosterone-like hormones) that are secreted by the adrenal glands during fetal life. (The condition is generally recognized and successfully treated after birth.) Affected girls are often born with some degree of masculinization of the external genitalia, in which case the condition is considered a form of intersexuality. Numerous studies have reported that CAH-affected girls tend to display a variety of gender-atypical traits (Berenbaum, Duck et al. 2000), though the effects may be small (Henderson and Berenbaum 1997). When adult they are much more likely to have experienced or to wish for homosexual relationships that comparison groups of women such as their unaffected sisters (Dittmann, Kappes et al. 1992).

Comment: Although it’s been suggested that the tendency toward gender-atypicality and homosexuality in CAH-affected females is an indirect effect caused by their (or their family’s) reaction to the partially masculinized genitalia, it seems more likely to be a direct effect of the prenatal androgens on brain development. Supporting this conclusion is the observation that there seems to be no relationship between the degree of genital masculinization and the degree of psychological gender-atypicality (Berenbaum and Bailey 2003). Of course, CAH is a rare condition and plays no role in the psychosexual development of most lesbian or bisexual women, but it supports the hypothesis that atypical prenatal hormone levels can influence adult sexual orientation.

 

Diethylstilbestrol (DES) exposure. DES is a synthetic, non-steroidal drug that activates estrogen receptors. It was widely prescribed to pregnant women before 1971. Women who were exposed to the drug during fetal life are significantly more likely to experience same-sex attraction than comparison groups such as their unexposed sisters, according to one small study (Meyer-Bahlburg, Ehrhardt et al. 1995), but a recent larger study found that exposed women were actually slightly less likely to have experienced a same-sex relationship (Titus-Ernstoff, Perez et al. 2003).

  Comment: The equivocal or possibly non-existent effect of prenatal DES on female sexual orientation, which contrasts with the strong effects seen in CAH, may reflect the fact that DES does not activate androgen receptors. Although androgens are normally converted to estrogens in the brain and thus activate estrogen receptors as well as androgen receptors, the direct activation of androgen receptors may be more important for this particular gendered trait, and perhaps for others too.

 

Prenatal stress theory of male homosexuality. Stressing pregnant rats (for example, by close confinement and exposure to bright lights) causes the male offspring of those pregnancies to display atypical sex behavior in adulthood: they are relatively unwilling to mount females and they may show a female-type response (“lordosis”) to being mounted by males (Ward 1972; Ward, Ward et al. 1994). The reason is that the stress activates the fetuses’ stress hormones which in turn lead to a diminution in the levels of testosterone during a critical period of brain development.

On the basis of Ward’s findings and his own animal studies, Dörner proposed that the mothers of homosexual men were exposed to severe stress during pregnancy, and he carried out retrospective studies that seemed to offer strong support for the hypothesis (Dörner, Geier et al. 1980; Dörner, Schenk et al. 1983). But more recent studies have either completely failed to confirm Dörner’s hypothesis (Schmidt and Clement 1990; Bailey, Willerman et al. 1991) or have provided very equivocal support for it (Ellis, Ames et al. 1988). Prenatal stress also has no effect on the development of gender role behavior in boys (Hines, Johnston et al. 2002).

Comment: The prenatal stress theory of male homosexuality seems to be incorrect, in spite of the animal results. Rats and humans probably differ in their stress-response mechanisms.

 

Effects on anatomy, brain structure and function, and cognition. Prenatal sex hormones have numerous effects on the developing body and brain. Thus, if there are differences in the levels of these hormones between pre-gay and pre-straight fetuses, one might expect to see other differences between gay and straight adults than simply their sexual orientation. Presumably, this would particularly likely for traits that differ between the sexes. Numerous studies have compared body anatomy, brain anatomy, brain function, and cognitive and personality traits between gay and straight men and between lesbian and heterosexual women. The results of some of these studies are reviewed in the following sections.

Anatomy

Penis size. According to a re-analysis of old Kinsey Institute data derived from about 5,000 men, the penises of gay men are slightly but significantly longer (6.46 vs. 6.14 inches measured along the top surface) and fatter than those of straight men (Bogaert and Hershberger 1999).

                      Comment: These findings are open to criticism because the measurements were made by the subjects themselves at home and not by an independent observer. (Gay men might be more tempted to exaggerate than straight men, or they might be more aroused by the sight of their erect penises, thus causing stronger erections.)  If correct, the result is inconsistent with the simplest form of the prenatal hormone hypothesis, which would predict gay men’s penises to be smaller. There are various ways one could make the findings fit the hypothesis, but it may not be worth dwelling on this until a replication study has been done—which could be a while.

 

Finger length ratios. In men the index finger (D2) is usually significantly shorter than the ring finger (D4), whereas in women D2 is nearly as long as D4. In other words, the D2:D4 ratio is usually lower in men than in women. Presumably this results from hormonal differences between males and females during development of the fingers. This idea is supported by the observation that CAH-affected individuals, who were exposed to high prenatal androgen levels, have low D2:D4 ratios (Brown, Hines et al. 2002).

Several groups have reported that the D2:D4 ratio is lower in lesbians than in heterosexual women (Williams, Pepitone et al. 2000; McFadden and Shubel 2002; Rahman and Wilson 2003), consistent with the prenatal hormone theory. It’s also been reported that only one subgroup of lesbians, namely those who self-identify as “butch” (masculine), has low D2:D4 ratios (Brown, Finn et al. 2002). This is one of the very few biological studies that look at the important differences that exist within the categories of “gay” and “lesbian.”

One study failed to confirm the relationship between D2:D4 ratios and sexual orientation in women, citing ethnicity as a confounding variable (Lippa 2003). The finding was confirmed, however, in another recent study that focused on female monozygotic twins who were discordant for sexual orientation: the lesbians twins had a lower 2D:4D ratio than their heterosexual co-twins (Hall and Love 2003). This suggests that the 2D:4D effect is independent of genes.

Data for men have been inconsistent: gay men have been reported to have a D2:D4 ratio that is lower (McFadden and Shubel 2002; Rahman and Wilson 2003), higher (Lippa 2003) or the same (Williams, Pepitone et al. 2000) as in straight men.

 

Fingerprints. A 1994 study reported a difference in the fingerprint patterns of gay and straight men: more specifically, the ratio of the numbers of ridges on the fingers of the left and right hands, which usually favors the right hand, was reported to be left-shifted in gay men (Hall and Kimura 1994). Two subsequent studies have failed to replicate this finding, however (Forastieri, Andrade et al. 2002; Mustanski, Bailey et al. 2002).

               Comment: None of these anatomical studies inspire tremendous confidence, though the D2:D4 findings in women seem the best documented, and are consistent with the prenatal hormone theory.

Brain studies—anatomy

Suprachiasmatic nucleus (SCN). This is a small group of cells in the hypothalamus that plays a key role in the generation of circadian rhythms. A Dutch group has reported that the SCN is larger in gay men than in straight men (Swaab and Hofman 1990).

Comment: This finding hasn’t been replicated (or refuted) by other labs. If it is correct, its significance is unclear since the SCN is not known to play a role in the generation of sexual feelings or behaviors.

Third interstitial nucleus of the anterior hypothalamus (INAH1). This small group of cells lies in a region of the hypothalamus called the medial preoptic area, which is known from animal studies to be involved in the generation of male-typical sex behavior. It is generally larger in men than women (Allen, Hines et al. 1989; LeVay 1991; Byne, Tobet et al. 2001). In a 1991 autopsy study, I reported that INAH3 was smaller, on average, in gay men than in straight men (LeVay 1991). A more recent study replicated this finding, although the magnitude of the difference was less (Byne, Tobet et al. 2001). This latter study also reported that there was a difference in cell density—a higher density (more cells per cubic millimeter) in the gay men. The researchers commented that the total number of cells in INAH3 may be the same in gay and straight men, but are packed more closely in the gay men, perhaps because they did not form so many synapses during development.

     Comment: There has been concern that the small size of INAH3 in the gay men might be a consequence of the disease (AIDS) from which most of them died, rather than their sexual orientation. However, neither I nor Byne’s group found any evidence that AIDS by itself has any effect on the size of INAH3. The findings on INAH3 support the prenatal hormone theory, because it’s known that manipulating testosterone levels in rats, if performed during a critical prenatal/perinatal period of development, affects the ultimate size of the analogous cell group in the rat’s hypothalamus, (Rhees, Shryne et al. 1990), as well as causing atypical sex behavior in adulthood (Grady, Phoenix et al. 1965).  Still, the findings don’t absolutely compel us to accept that prenatal events influence sexual orientation, since (as mentioned above) there is evidence that some sexually dimorphic brain structures can be modified by hormonal or other changes in adulthood.

            A group at the Oregon Health Sciences University recently reported analogous findings for sheep (Roselli, Larkin et al. 2004). A hypothalamic cell group that may be the sheep equivalent of INAH3 was reported to be larger in rams than ewes, but smaller in rams that mate exclusively with other rams (“homosexual rams”) than in heterosexual rams. The cell group also expressed lower levels of aromatase—the enzyme that converts testosterone to estrogen—in the homosexual rams than in the heterosexual rams.

            Comment: Of course I like this study because it offers such a close parallel to my own human study. Why some rams are homosexual is not known—exclusive homosexuality seems to be rare in the animal kingdom—but there are other studies suggestive of a neuroendocrinological mechanism (Pinckard, Stellflug et al. 2000).

     There is a report that the anterior commissure, a fiber bundle connecting the left and right sides of the cerebral cortex, is larger in women than men, and larger in gay men than in straight men (Allen and Gorski 1992).

Comment: This report has not been replicated or refuted. The significance of the finding, if correct, is unclear, though it might be related to the cognitive differences that have been reported between gay and straight men (see below).

NEW! The Karolinska group (Ivana Savic and Per Lindstrom) reported on the relative sizes of the left and right cerebral hemispheres in gay and straight men and women, as determined from MRI scans (Savic and Lindstrom 2008). In straight men, the right hemisphere is about 2 percent larger than the left hemisphere, on average, whereas in straight women the two hemispheres are the same size. In gay people, it’s the reverse: gay men have symmetrical hemispheres, and lesbians have a larger right hemisphere. In the same paper the researchers examined the connections of the left and right amygdalas—brain regions that are involved in the processing of emotions. The connections were determined by PET scanning. (If two brain regions are interconnected, cerebral blood flow—which PET measures—tends to be correlated in time between the two regions.) The connectivity patterns of the two amygdalas were asymmetrical and different between heterosexual men and women. For example, the right amygdala has more connections than the left in heterosexual men, whereas in women the left amygdala has more connections that the right amygdala. Again, these asymmetries were sex-atypical in gay men and women.

Comment: This seems to offer two more examples of sex-atypical brain organization in gay people. The findings are consistent with the idea that some common driver, such as prenatal hormone levels, guides the development of a package of gender-related brain systems in a sex-atypical direction in fetuses that later become gay men and women.

Brain studies—function

Auditory system. There are differences between men and women in the functional properties of the inner ear and the central auditory system, as assessed by measurement of otoacoustic emissions (sounds produced by the inner ear) and auditory evoked potentials (recordings of brain activity following a brief sound). Dennis McFadden and his colleagues (McFadden 2002) have reported that lesbian and bisexual women have partially masculinized otoacoustic emissions and auditory evoked potentials. They also report that women who had male twins (and who may therefore have been exposed to testosterone from their twin during prenatal life) are likewise masculinized in otoacoustic emissions, as mentioned above. They therefore interpret their findings as consistent with the prenatal hormonal theory of sexual orientation, i.e., that pre-lesbian or pre-bisexual fetuses are exposed to atypically high levels of androgens. Interestingly, the researchers found no difference in the otoacoustic emissions of gay and straight men, but they observed that some aspects of the evoked potentials of gay men were shifted in a “hypermasculine” direction—which if true is the opposite of what would be expected on the basis of the prenatal hormone theory, at least in its simplest form.

A British group (Rahman, Kumari et al. 2003) recently reported differences in the startle response (eyeblink following a loud sound) of lesbians compared with heterosexual women. It was previously known that men and women differ in the extent to which the startle response is inhibited when the loud sound is preceded by a weaker sound: this “prepulse inhibition” (PPI) is typically less evident in women than men. The researchers reported that the PPI was greater (i.e., masculinized) in the lesbian subjects, a finding that they interpreted in terms of the prenatal hormone theory. They did not find any difference between the startle responses of gay and straight men.

Comment: These specific findings await independent replication, but the Rahman and McFadden studies are consistent with each other.

 

Sexual arousal. A brief report from Bailey and Mesulam’s groups described the patterns of brain activity in gay and straight men while they were viewing sexually arousing and non-arousing images (Barch, Reber et al. 2003). The regions selectively active during arousing stimuli were generally the same ones in the two groups, but three regions (medial prefrontal cortex, left hippocampus, and right amygdala) were more selectively active in the gay men.

      Comment: Probably the main message of this study is the similarity of activity patterns in the gay and straight men during sexual arousal, in spite of the differences in the kind of images they find arousing.

 

Neurotransmitter function. A group at the University of Chicago (Kinnunen, Moltz et al. 2004) compared the brain’s metabolic response to oral administration of a selective serotonin reuptake inhibitor, fluoxetine, in gay and straight men. Using fluorodoxyglucose positron emission tomography, they found differences in response in several brain regions. In the hypothalamus, the heterosexual men showed a significantly greater reduction of glucose metabolism in response to the drug, though only on the right side.

            Comment: It could be that the serotonergic input to INAH3 is less extensive in gay men, corresponding to the smaller size of this cell group. However, PET imaging does not permit resolution of individual hypothalamic nuclei. Also, the lateralization of the effect is puzzling. The researchers did not test for a basic sex difference in fluoxetine responses.

 

Odor responses. A group at the Karolinska Institute has previously reported differences in the patterns of brain activity between heterosexual men and women when smelling two putative human sex pheromones, 4,16-androstadien-3-one (AND)(a component of male armpit secretions) and estra-1,3,5(10),16-tetraen-3-ol (EST)(found in female urine). In PET scans, men showed activity in the anterior hypothalamus during exposure to EST but not to AND (Savic, Berglund et al. 2001), while women showed hypothalamic activity during exposure to AND but not EST (The location of activity within the hypothalamus was slightly different.) In a recent follow-up the research group included homosexual men in a similar experiment (Savic, Berglund et al. 2005). They found that gay men had a pattern of hypothalamic activity resembling that of heterosexual women: activity was elicited by AND and not EST. In contrast, activity patterns in the olfactory cortex were similar in all three groups. The researchers suggest that the hypothalamus is organized to respond to sex pheromones in a sex-atypical way in homosexual men.

Recently the Swedish group reported on a similar study comparing heterosexual and lesbian women (Berglund, Lindstrom et al. 2006). As might be expected, they found that AND elicited activity in the anterior hypothalamus of heterosexual women but not lesbians. The results with EST were more equivocal but were more similar to those observed in heterosexual men than in heterosexual women.

In a related study, researchers at the Monell Chemical Senses Center tested the preferences of heterosexual men, homosexual men, heterosexual women, and homosexual women for armpit secretions pooled from six-member panels representing these same four subject groups (Martins, Preti et al. 2005). They reported differences in preferences related to both the sex and the sexual orientation of both the donor panels and the judging panels. For example, gay men preferred odors from gay men to those from other groups, whereas straight men like the odor from gay men less than from other groups. The authors suggest that biological factors lead to recognizably different odors in persons of the same sex but different sexual orientation, and that homosexual men and women assess the attractiveness of these odors differently.

                    Comment: The question of human sex pheromones has been controversial, in part because the biological system that detects sex pheromones in mammals (the vomeronasal system and its molecular receptors and neural connections) appear to be missing, vestigial, or non-functional in humans. It should be noted that the “pheromones” in the Swedish study were presented in very high and uncontrolled concentrations, so that they could be consciously perceived as odors.  Thus the results, though consistent with the idea that a sex-pheromone system is wired up differently in homosexual and heterosexual men, could also be interpreted as reflecting sexual arousal or non-arousal induced by odors that the subjects have come to recognize as belonging to their preferred or non-preferred partners—similar to the activity patterns that might be elicited by, for example, erotic videos featuring men or women. Nevertheless, it has been shown that both AND and EST activate the human hypothalamus when presented at concentrations below the threshold for conscious perception. If the Swedish results related to sexual orientation could be replicated with sub-threshold concentrations of the odorants, this would bolster the idea that a pheromonal mechanism is at work.

 The Monell study suggests that gay and straight people emit different armpit odors, possibly as a result of biological differences in the major histocompatibility complex (MHC) genes or something similar, but other explanations are possible. Given that the donor panels were so small these results need to be replicated. The preference shown by gay men for the odors derived from gay men, if it holds up, seems more likely to be a learned response that an innate biological mechanism, because there is no evidence that gay men have an innate preference for gay male partners over straight male partners.

Cognitive studies

General. Men and women differ in a number of cognitive traits. Men tend to outperform women in certain kinds of visuospatial tasks, such as mental rotation and targeting, as well as in mathematical reasoning, whereas women tend to outperform men in tests of verbal fluency (speed at coming up with words that correspond to some category), speed of calculation, recognition of facial expressions, and memory of object location (Kimura 1999). In navigation tasks, women typically use landmark cues more than men do. Men are also typically more competitive and aggressive than women. There is evidence that these sex differences result at least in part from differences in prenatal sex hormone levels (Collaer and Hines 1995). Thus, in terms of the prenatal hormone hypothesis it makes sense to ask whether gay people differ from straight people of the same sex in any of these traits.

 

Visuospatial tasks. A number of studies have reported that gay men perform worse than straight men on a variety of visuospatial tasks, such as mental rotation, judgment of line orientation, and targeting (Gladue, Beatty et al. 1990; McCormick and Witelson 1991; Hall and Kimura 1995; Wegesin 1998; Neave, Menaged et al. 1999; Rahman and Wilson 2003). In these studies the gay men performed at the female-typical level or at an intermediate level. Two studies failed to find differences between gay and straight men (Gladue, Beatty et al. 1990; Tuttle and Pillard 1991). In navigation tasks gay men, like heterosexual women, use landmark cues much more than heterosexual men do (Rahman, Andersson et al. 2005). Findings for women have been mixed: one recent large study found that lesbians are moderately better than heterosexual women at mental rotation, but the difference was only in speed of response, not accuracy (Rahman and Wilson 2003).

 

Object location memory. One recent large study of object location memory found that gay men do better than straight men, and about at the level of heterosexual women. No difference between the performance of lesbian and heterosexual women was found (Rahman, Wilson et al. 2003).

 

Verbal fluency. A 1991 study reported that gay men outperform heterosexual men in this trait (McCormick and Witelson 1991). Two subsequent studies came up with negative results (Gladue, Beatty et al. 1990; Neave, Menaged et al. 1999), but a recent large study reported that both gay men and lesbians have sex-atypical scores in verbal fluency tests (Rahman, Abrahams et al. 2003).

 

Aggressiveness. Gay men are reported to be less physically aggressive than straight men (Ellis, Hoffman et al. 1990; Gladue and Bailey 1995). No difference was found between lesbians and straight women (Gladue and Bailey 1995).

 

Handedness. There seems to be little or no difference in the handedness of heterosexual men and women (Lippa 2003), but most studies have found that gay men and/or lesbians are significantly more likely to be non-righthanded (i.e. left-handed or mixed-handed) than straight people of the same sex (Lalumiere, Blanchard et al. 2000; Mustanski, Bailey et al. 2002; Lippa 2003).

               Comment: Hand preference is observable before birth (Hepper, Shahidullah et al. 1991), though it can change as a result of birth trauma and the like. The observation of increased non-righthandness in gay people is therefore consistent with the idea that sexual orientation is influenced by prenatal processes.  

Birth order

A considerable number of studies, mostly by a Canadian group of researchers, have reported that gay men tend to have more older brothers than do straight men (Blanchard and Bogaert 1996; Bogaert 2003). By way of explanation, the researchers hypothesize that some women develop antibodies to male-specific antibodies during early pregnancies with male fetuses, and that these antibodies affect the development of subsequent male fetuses in such a way as to increase the likelihood of homosexuality. This might happen through a general retardation of fetal growth with resulting small stature in postnatal life (Bogaert 2003).

The Canadian group has reported that the birth order effect is seen only among right-handed men (Blanchard, Cantor et al. 2006). Being non-righthanded, even though by itself it increases the likelihood of being gay (see above), actually nullifies the gay-promoting influence of older brothers. The authors speculate that this might be because the two causal factors work to make a fetus gay through opposing mechanisms: by raising prenatal androgen levels in one case and lowering them in the other, for example, so that when the two causal factors are combined androgen levels end up within the range that promotes heterosexuality.

       Comment: The birth-order effect seems to be robust across numerous samples. It is not a particularly large effect, however: it would take an improbable number of older brothers (I think about 10) to give a boy even a 50:50 chance of being gay by the birth-order effect alone. In general, birth-order effects on psychological traits are explained by family dynamics (e.g., in this case, by parents “permitting” younger sons to be gay). However, the researchers have offered some good arguments why family dynamics are not likely to be the main explanation in the case of sexual orientation. For example, Bogaert reported that non-biological older brothers have no effect, while biological older brothers do have an effect even if they never lived with the proband (Bogaert 2006). A more direct test of their hypothesis, such as the detection of anti-male antibodies in the mothers of gay men, remains to be done.

 

General comments

Although quite a few of the findings reported here are inconsistent between studies or await independent replication, my general conclusion is that biological processes, especially the prenatal, hormonally-controlled sexual differentiation of the brain, are likely to influence a person’s ultimate sexual orientation.

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