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The Biology of
Sexual Orientation
© Simon LeVay, 2003. Latest update: June 2008
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).
Contents:
Non-biological theories
Biological theories
Non-biological theories
Psychoanalytic
theories
Early in the 20th 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 20th
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”).
2.
A gene might
cause homosexuality and thus reduce reproductive success when present on two
homologous chromosomes (homozygous state) but have some other, positive effect when
present on one chromosome (heterozygous state). The analogy is to the
sickle-cell gene which causes anemia when homozygous but confers resistance to
malaria when heterozygous. If the heterozygous advantage is sufficiently great
the gene will persist in the population.
3.
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).
4.
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.
5.
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