A. The Charge. The Darwinian theory of evolution is now generally accepted as the definitive account of the origin and development of life’s many varieties, including human life. Yet homosexual behavior is not compatible with this overarching theory. It remains an anomaly.
B. Background. In the current approach known as evolutionary biology the inclusive fitness of an organism is the sum of its classical fitness (that is, how many of its own offspring it produces and supports) and the number of equivalents of its own offspring it can add to the population by supporting others. Advocates of inclusive fitness theory hold that an organism can improve its overall genetic success by cooperative social behavior.
From the gene's point of view, evolutionary success ultimately depends on leaving behind the maximum number of copies of itself in the population. Until 1964, it was generally believed that genes only achieved this goal by causing the individual to leave the maximum number of viable offspring. However, in 1964 W. D. Hamilton demonstrated mathematically that, because close relatives of an organism share some identical genes, a gene can also increase its evolutionary success by promoting the reproduction and survival of these related or otherwise similar individuals.
How does this principle relate to homosexual behavior? Sexual practices that significantly reduce the frequency of heterosexual intercourse also decrease the chances of successful reproduction, and for this reason, they would appear to be maladaptive in an evolutionary context. At least that would be so with a model that follows a simple Darwinian model of natural selection - on the assumption that homosexuality would reduce this reproductive frequency. Several theories have been advanced to explain this contradiction, and new experimental evidence lends them plausibility.
Some scientists have suggested that homosexuality is adaptive in a non-obvious way. By way of analogy, the allele (a particular version of a gene) which causes sickle-cell anemia when two copies are present may also confer resistance to malaria with a lesser form of anemia when one copy is present (this is called heterozygous advantage).
The so-called "gay uncle" hypothesis posits that people who themselves do not have children may nonetheless increase the prevalence of their family's genes in future generations by providing resources (food, supervision, defense, shelter and the like) to the offspring of their closest relatives. This hypothesis is an extension of the theory of kin selection.
Kin selection was originally developed to explain apparent altruistic acts which seemed to be maladaptive. Proposed by J.B.S. Haldane in 1932, the concept was later elaborated by others, including John Maynard Smith, W. D. Hamilton and Mary Jane West-Eberhard. The concept also served to explain the survival strategies of certain social insects where most of the members are non-reproductive.
Brendan Zietsch of the Queensland Institute of Medical Research has proposed an alternative theory to the effect that men exhibiting female traits become more attractive to females and are thus more likely to mate, provided the genes involved do not drive them to complete rejection of heterosexuality.
In a 2008 study published in the journal Evolution and Human Behavior [29 (6): 424–433], its authors stated that "There is considerable evidence that human sexual orientation is genetically influenced, so it is not known how homosexuality, which tends to lower reproductive success, is maintained in the population at a relatively high frequency." They hypothesized that "while genes predisposing to homosexuality reduce homosexuals' reproductive success, they may confer some advantage in heterosexuals who carry them." and their results suggested that "genes predisposing to homosexuality may confer a mating advantage in heterosexuals, which could help explain the evolution and maintenance of homosexuality in the population." However, in the same study, the authors noted that "nongenetic alternative explanations cannot be ruled out" as a reason for the heterosexual in the homosexual-heterosexual twin pair having more partners, specifically citing "social pressure on the other twin to act in a more heterosexual way" (and thus seek out a greater number of sexual partners) as an example of one alternative explanation. Also, the authors of the study acknowledge that a large number of sexual partners may not lead to greater reproductive success, specifically noting there is an "absence of evidence relating the number of sexual partners and actual reproductive success,either in the present or in our evolutionary past."
Significant new evidence on a plausible mechanism for the evolution of "gay genes" has emerged from the work of Andrea Camperio-Ciani and his colleagues. In two large, independent studies they found that the female relatives of homosexual men tended to have significantly more offspring than those of the heterosexual men. Female relatives of the homosexual men on their mother's side tend to have more offspring than those on the father's side. This indicates that females carrying a putative "androphilia genes" complex are more fecund than women lacking this complex of genes, and thereby can compensate for any decreased fertility of the males carrying the genes. This is a well known phenomenon in evolution known as "sexual antagonism," and has been widely documented for many traits that are advantageous in one sex but not in the other. This research provides experimental evidence of how "gay genes" could not only survive but thrive over the course of evolution.
C. Response. While these research findings are suggestive, it is not certain that they truly resolve the Darwinian problem of how exclusive homosexuals can continue to appear over the generations. Of course, it may be that the etiology is simply cultural. If so, though, how is it that homosexuality has appeared independently in so many human groups, not to mention many species of animals? Some puzzles simply remain, at least in the present state of knowledge.
BIBLIOGRAPHY. James D. Weinrich, Sexual Landscapes, New York: Charles Scribner's Sons, 1987, Michael Ruse, Homosexuality: A Philosophical Inquiry, Oxford: Blackwell, 1988; Andrea Camperio-Ciani, F. Corna, and C. Capiluppi, “Evidence for Maternally Inherited Factors Favouring Male Homosexuality and Promoting Female Fecundity,” Proceedings of the Royal Society, London B, vol. 271, no. 1554 (Nov. 7, 2004), 2217-21.