by Kenneth W. Krause.
Kenneth W. Krause is a contributing editor and “Science Watch” columnist for the Skeptical Inquirer. Formerly a contributing editor and books columnist for the Humanist, Kenneth contributes regularly to Skeptic as well. He may be contacted at email@example.com.
The persistence of homosexuality among certain animal species, including humans, has bewildered scientists at least since the time of Darwin. Why should same-sex attraction persist when evolution assumes reproductive success? Does homosexuality—especially among humans—facilitate the intergenerational transfer of genetic material in some other way? Or perhaps it advances an entirely different objective that justifies it’s more obvious procreative disadvantage. Such questions have long attracted gene-based explanations for homosexuality.
Consider “kin selection,” for example. As E.O. Wilson first suggested in 1975, maybe human homosexuals are like sterile female worker bees that assist the queen in reproduction. One study of homosexual men, known in Independent Samoa as fa’afafine, revealed that gays are significantly more likely than straight men to help their siblings raise children.
But to satisfy the kin selection hypothesis, each gay must account for the survival of at least two sibling-born children for every one he fails to reproduce—a difficult standard to attain accomplish. In any case, relevant studies in the U.S. and U.K. have failed to provide such evidence.
As a possible explanation for male homosexuality, other researchers have offered the “fertile female” hypothesis. Here, a genetic tendency toward androphilia, or attraction to males—though problematic for men from an evolutionary perspective—is thought to enhance the reproductive success of their straight, opposite-sex relatives by rendering them hyper-sexual.
At least two studies have claimed results in support of the fertile female model. Notably, this hypothesis is also capable of explaining why gayness persists at a constant but low frequency of about eight percent in the general global population.
A former faculty member at Harvard Medical School and the Salk Institute, neuroscientist Simon LeVay favors evidence suggesting a suite of several “feminizing” genes (LeVay 2011). The inheritance of a limited number of these genes, LeVay proposes, will make males, for instance, more attractive to females—and thus presumably more successful in terms of reproduction—by rendering them less aggressive and more empathetic, for example.
But a few men in the family tree will receive “too many” feminizing genes and, as a result, be born gay. Indeed, one Australian study has discovered that gender-atypical traits do enhance reproduction, and that heterosexuals with homosexual twins achieved more opposite-sex partnerships than heterosexuals without homosexual twins—though statistical significance was observed only among females.
Even so, most explanations are not based solely in genetics. Evidence suggests as well, for example, that a variety of mental gender traits are shaped during fetal life by varying levels of circulating sex hormones. Especially during certain critical periods of development, testosterone (T) levels in particular are thought to cause the brain to organize in a more masculine or feminine direction and, later in life, to influence a broad spectrum of gender traits including sexual preference.
For instance, women suffering from congenital adrenal hyperplasia due to elevated levels of prenatal T and other androgens are known to possess gender traits significantly shifted toward masculinity and lesbianism. Importantly, female fetuses most severely affected by CAH and, thus, most heavily exposed to prenatal androgens are the most likely to experience same-sex attraction later in life.
Similarly, the bodies of male fetuses afflicted with androgen insensitivity syndrome—a condition in which the gene coding for the androgen receptor has mutated—will fail to react normally to circulating T. As a result, these XY fetuses will later appear as girls and, as adults, share an attraction to men. In sum, although a number of other factors could be, and likely are, at play, it is now fairly well established that prenatal androgen levels have a substantial impact on sexual orientation in both men and women.
But three researchers working through the National Institute for Mathematical and Biological Synthesis have recently combined evolutionary theory with the rapidly advancing science of both androgen-dependent sexual development and molecular regulation of gene expression to propose a new and provocative epigenetic model to explain both male and female homosexuality (Rice, et. al. 2012).
According to lead author William Rice at the university of California, Santa Barbara, his group’s hypothesis succeeds not only in squaring homosexuality with natural selection—it also explains why same-sex attraction has been proven substantially heritable even though, one, numerous molecular studies have so far failed to locate associated DNA markers and, two, concordance between identical twins—about twenty percent—is far lower than genetic causation might predict.
At the model’s heart are sex-specific epigenetic modifications, or epi-marks. Generally speaking, epi-marks can be characterized as molecular regulatory switches attached to genes’ backbones that direct how, when, and to what degree genetic instructions are carried out during an organism’s development. They are created anew during each generation and are usually “erased” between generations.
But because epi-marks are produced at the embryonic stem cell stage of development—prior to division between soma and germline—they can in theory be transmitted across generations. Indeed, some evidence does suggest that on rare occasions (though not at scientifically trivial rates) they will carry over, and thus mimic the hereditary effect of genes.
Under typical circumstances, Rice instructs, sex-specific epi-marks serve our species’ evolutionary objectives well by canalizing subsequent sexual development. In other words, they protect sexually essential developmental endpoints by buffering XX fetuses from the masculinizing effects and XY fetuses from the feminizing effects of fluctuating in utero androgen levels. Significantly, each epi-mark will influence some sexually dimorphic traits—sexual orientation, for example—but not others.
According to the new model, however, when sex-specific epi-marks manage to escape intergenerational erasure and transfer to opposite-sex offspring, they become sexually antagonistic (SA) and thus capable of guiding the development of sexual phenotypes in a gonad-discordant direction. As such, Rice hypothesizes, “homosexuality occurs when stonger-than-average SA-epi-marks (influencing sexual preference) from an opposite-sex parent escape erasure and are then paired with weaker-than-average de novo sex-specific epi-marks produced in opposite-sex offspring.”
To summarize, Rice’s team argues that differences in the sensitivity of XY and XX fetuses to the same levels of T might be caused by epigenetic mechanisms. Normally, such mechanisms would render male fetuses comparatively more sensitive and female fetuses relatively less sensitive to exposure. But if such epigenetic labels pass between generations, they can influence sexual development. And if they pass from mother to son or from father to daughter, sexual development can proceed in a manner that is abnormal (or “atypical,” if you prefer). In those very exceptional cases, offspring brain development can progress in a fashion more likely to result in homosexuality.
Rice’s observations and insights are fascinating, to say the least. Indeed, popular news reports describe a scientific community highly appreciative of the new model’s theoretical power. Nevertheless, a great deal of criticism has been tendered as well.
LeVay, for example, describes the authors’ hypothesis generally as “a reasonable one that deserves to be tested—for example by actual measurement of the epigenetic labeling of relevant genes in gay people and their parents.” He reminded me, however, that Rice hasn’t actually discovered anything. The new model is in fact pure speculation, says LeVay, and it never should have been reported—as some media have done—as “the cause” (or even as “a cause”) of homosexuality.
More specifically, LeVay offers three points of caution. First, he warns that an epigenetic explanation is not to any degree implied from the current data on fetal T levels. When based on single measurements, he concedes, male and female fetuses may indeed show some overlap. But because T levels fluctuate in both males and females throughout development, allegedly anomalous individuals might easily average completely sex-typical T levels over time. Second, LeVay sees “little or no evidence” that epi-marks ever escape erasure in humans.
Finally, LeVay continues to favor genetic explanations. The incidence of homosexuality in some family trees, he says, is more consistent with DNA inheritance than with any known epigenetic mechanism. Moreover, he warns, we should never underestimate the difficulty of identifying genetic influences—especially with regard to mental traits. In such cases, complex polygenic origins are far more likely to be at play than single, magic genetic bullets.
Other neuroscientists have posed equally important questions. How can we test whether the appropriate epi-marks—probably situated in the brain—have been erased? Is it too simplistic to suggest identical or even similar mechanisms for both male and female homosexuality? Why is it important to isolate the specific biological causes of same-sex attraction? By doing so, do we run the risk of further stigmatizing an already beleaguered population?
Rice doesn’t deny his new model’s data deficit. Nor does he portray the epigenetic influence on same-sex attraction as an exclusive one. His team does, however, insist that epigenetics is “a probable agent contributing to homosexuality.” We now have “clear evidence,” they maintain, that “epigenetic changes to gene promoters … can be transmitted across generations and … can strongly influence, in the next generation, both sex-specific behavior and gene expression in the brain.”
The authors contend as well that their hypothesis can be rapidly falsified because it makes “two unambiguous predictions that are testable with current technology.” First, future large-scale association studies will not identify genetic markers correlated with most homosexuality. Any such associations found, they say, will be weak.
Second, future genome-wide epigenetic profiles will distinguish differences between homosexuals and non-homosexuals, but only at genes associated with androgen signaling or in brain regions controlling sexual orientation. Testing this second prediction, they admit, may proceed only with regard to lesbianism by comparing profiles of sperm from fathers with and without homosexual daughters.
To my knowledge, Rice and his colleagues have never squarely addressed the question of whether, for philosophical or sociological reasons, we should refrain from delving further into the dicey subject of same-sex attraction. Such questions do, however, expose a tendency toward communal repression and a general lack of respect for the scientific enterprise. These decisions should be left to the scientists and those who fund them.
LeVay, Simon. 2011. Gay, Straight, and the Reason Why: The Science of Sexual Orientation. NY: Oxford University Press.
Rice, W., Friberg, U., and Gavrilets, S. 2012. Homosexuality as a consequence of epigenetically canalized sexual development. The Quarterly Review of Biology 87(4): 343-368.