Male Homosexual Preference: Where, When, Why? (PLoS ONE):
Male homosexual preference (MHP) has long been of interest to scholars studying the evolution of human sexuality. Indeed, MHP is partially heritable, induces a reproductive cost and is common. MHP has thus been considered a Darwinian paradox. Several questions arise when MHP is considered in an evolutionary context. At what point did MHP appear in the human evolutionary history? Is MHP present in all human groups? How has MHP evolved, given that MHP is a reproductively costly trait? These questions were addressed here, using data from the anthropological and archaeological literature. Our detailed analysis of the available data challenges the common view of MHP being a “virtually universal” trait present in humans since prehistory. The conditions under which it is possible to affirm that MHP was present in past societies are discussed. Furthermore, using anthropological reports, the presence or absence of MHP was documented for 107 societies, allowing us to conclude that evidence of the absence of MHP is available for some societies. A recent evolutionary hypothesis has argued that social stratification together with hypergyny (the hypergyny hypothesis) are necessary conditions for the evolution of MHP. Here, the link between the level of stratification and the probability of observing MHP was tested using an unprecedented large dataset. Furthermore, the test was performed for the first time by controlling for the phylogenetic non-independence between societies. A positive relationship was observed between the level of social stratification and the probability of observing MHP, supporting the hypergyny hypothesis. [. . .]
Alternatively, the increase in fertility in a close relative could be the result of an antagonistic factor. A sexually antagonistic gene that favors MHP in males and that increases fecundity in females has been proposed . Several studies support this hypothesis [4, 22, 31–34] and other have provided results that are consistent with predictions from this hypothesis [22, 34–38]. However why such an effect would not operate also in wild animals is unclear. Sexually antagonistic genes are either fixed (when the advantage is higher than the cost) or selected against (when the cost is higher than the advantage). When the frequency of a sexually antagonistic gene increases, selection to decrease the cost could eventually operate (for example through the selection of a modifier gene), thus decreasing the fixation time of the antagonistic gene. In any case, such sexually antagonistic genes are only transiently observed in natural population, perhaps explaining the absence–so far–of reports of homosexual preference in wild animals. A recent change in social conditions could change the relative fitness advantage and cost of such gene, thus enhancing its selection.
It has been recently proposed that selection for such sexually antagonistic genes could be promoted in social contexts specific to some human societies, where there is social stratification and hypergyny (i.e., a bride marries a groom of higher social status) . Indeed in a stratified society, populations are organized into different groups (or classes) in which people share similar socioeconomic conditions. These groups can be ranked hierarchically depending on their access to resources (with more resources for the top class). This social inequality also affects the expected reproductive success of each group (with higher reproductive success associated with the top class) [40–45]. This hypergyny hypothesis posits that females carrying the sexual antagonistic variant (associated with MHP in males) will signal increased levels of fertility (through higher femininity or attractiveness), thereby increasing their probability of reproducing in a wealthier social environment. Such a sexually antagonistic gene will then provide a direct advantage (by increasing fertility) and an indirect advantage (by increasing the probability of marrying into higher social classes). Such a process may promote MHP in stratified societies, and indeed, a comparative analysis suggests that social stratification level is a predictor of the presence of MHP in a society . Several potential confounding variables were considered in this analysis, with the conclusion that none of them significantly influenced the probability of report of homosexual preferences. These variables included population density (a good proxy of the number of indigenous people met by the anthropologist), geographical location and presence of moralizing gods. However, this comparative study considered only 48 societies, and phylogenetic dependence among them (Galton's problem)  was not clearly addressed. [. . .]
Contrary to the widely held view that MHP is present in all contemporary societies e.g., [20, 22], the anthropological data gathered here show that MHP is likely absent from some societies, especially those that display low levels of stratification. Anthropologists that have explicitly searched for signs of MHP have acknowledged its absence: among the Alorese “The fact is that homosexuality as such is not known either among women or men” ; “Homosexuality and onanism are unknown among the Bororo, as well as among the majority of the Indian tribes visited by me” ; “Homosexuality is said to be unknown in Ulithi, but it is admitted as a possibility” ; among the Ifaluk people “The people know of no cases of homosexuality or of sexual perversions, nor did I observe any” ; and among the Yanomamö, “Most of the unmarried young men in Bisaasi-tedi were having homosexual relationships with each other […] The men involved in these affairs, however, were hardly more than teenagers; I have no cases of adult men satisfying their sexual needs by homosexuality” . The most recent account of the absence of MHP concerns the Aka people, a hunter-gatherer group from Central African Republic for which an anthropologist noted that “The Aka, in particular, had a difficult time understanding the concept and mechanics of same sex relationships. No word existed and it was necessary to repeatedly describe the sexual act. [. . .]
A predictor of the presence of MHP in a given society is the level of social stratification. This result remains well supported even when non-independence among societies modelled as linguistic or geographical proximities is accounted for and when two independent measures of stratification level (using the EA or eHRAF) were considered. In all cases, the probability of observing MHP increases with the level of social stratification. It is thus expected that several social variables directly related to stratification would also be associated with MHP. There have been previous attempts to identify social variables related to homosexuality . However, Barber did not distinguished male and female homosexuality, and did not differentiate between homosexual preference (MHP) and behavior, thus his results are not directly comparable to ours. Despite these caveats, Barber found several traits often associated with traditional stratified societies (large community size, agricultural food, low levels of female control over sex), that predict his measure of the homosexual frequency. Unfortunately, he did not studied directly the stratification level.
In stratified societies, MHP is most likely not selected for directly as it represents a fitness cost, but we hypothesize that it is associated with a pleiotropic and antagonist factor. It has been proposed that the fitness advantage of such a pleiotropic factor is an increase in female fertility , which would affect the probability of females marrying men from higher social classes in stratified societies . This effect of stratification level on the probability of observing MHP is thus consistent with the hypergyny hypothesis . The present data do not allow the trait under selection in stratified societies to be identified. One possibility that cannot be excluded is that other types of pleiotropic factors have been selected for, as long as fitness advantages are conferred in a socially stratified context. In any case, social stratification remains the only pivotal identified social variable (i.e., defined above the individual level) associated with MHP in a cross-cultural analysis.
MHP was observed in all highly stratified societies (with at least 5 levels of stratification) of the present sample. As social stratification has occurred independently in various parts of the globe, two scenarios can be proposed about the emergence of MHP. First it is possible that MHP arose independently in those stratified societies. In this case, the life-history traits associated with MHP may not be expected to be the same in different independent societies, depending on the exact nature of the pleiotropic factor that is the target of selection. Some data support this hypothesis, for example, the older brother effect, associated with MHP in Western societies ), is not exactly replicated in other stratified societies: in Samoa, MHP is associated with an “older sister” effect [38, 90]. This suggests that the pleiotropic and antagonistic factor expressing MHP is recurrent, although the pleiotropic factor may vary. Alternatively, the factors that favor MHP could have preexisted to the expansion of humans across the globe. In this case, the selection due to the effect of social stratification could have promoted the same preexisting factors that favor MHP. Thus, the life-history traits associated with MHP in the various highly stratified societies should be similar by descent. As an example of supportive data, the frequency of gender atypical behaviors during childhood is reported to be higher in MHP than in heterosexual men (on the basis of recall) in Brazil, Guatemala, the Philippines and the United States of America . This remains an open question, and more data are required. [. . .]
Social stratification remains the only known social variable significantly influencing the presence of MHP in a given society. This is consistent with the idea that a pleiotropic and antagonist factor is the target of selection in stratified societies and that MHP imposes a fitness cost on male fertility. Whether the selected trait is female fertility (under the hypergyny hypothesis) or another life-history trait has yet to be evaluated, although the selected trait may differ among various independent stratified societies. Data from pristine prehistoric societies (i.e., isolated from the influence of stratified societies) are currently non-existent. Unless other social variables (independent from social stratification) influencing MHP are identified, societies with low levels of stratification are predicted to display, at best, a low level of MHP individuals. Social stratification as a promoting factor of MHP is also consistent with currently available data showing that MHP seems to be absent in wild animals. This is because the type of social stratification displayed in humans has no equivalent in other animals. Human social stratification is defined across generations, and a given individual generally belongs to the same social class during his entire lifetime, and usually reproduces within the same class. The dominance rank in social non-human animals is generally transient (e.g. the tenure of the alpha chimpanzee lasts only few years, ) or, if transmitted to the next generation, restricted to one sex (e.g. female ranks among the spotted hyaena and some Cercopithecines species [97, 98]) [. . .]
Here we show that the commonly held view of the virtually universal presence of MHP since prehistoric time in human populations is not confirmed upon review of the cited data. Indeed, the existence of MHP in past times can never be proved or disproved using only archaeological remains: written texts are required to establish that homosexual preference was eventually present, and this information is probably definitively inaccessible for prehistoric (e.g., before written texts) societies. Today, MHP appears to be absent in some societies but present in others; this variability can be partly explained by the level of social stratification. This is consistent with a factor being selected for in a stratified society, despite a pleiotropic cost on functional male fertility (MHP). One possible candidate is a factor increasing female fertility, specifically by increasing the probability that a female marries males from higher social classes when hypergyny is enforced. As stratified societies are relatively recent (generally post-Neolithic), the substantial prevalence of MHP is most likely a recent phenomenon in humans and much remains to be understood.