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Study shows male homosexuality can be explained through a specific model of Darwinian evolution

June 17th, 2008 posted by Josh Hill

Reporting in this week’s PLoS ONE, an Italian research team, consisting of Andrea Camperio Ciani and Giovanni Zanzotto at the University of Padova and Paolo Cermelli at the University of Torino, found that the evolutionary origin and maintenance of male homosexuality in human populations could be explained by a model based around the idea of sexually antagonistic selection, in which genetic factors spread in the population by giving a reproductive advantage to one sex while disadvantaging the other.

Male homosexuality is thought to be influenced by psycho-social factors, as well as having a genetic component. This is suggested by the high concordance of sexual orientation in identical twins and the fact that homosexuality is more common in males belonging to the maternal line of male homosexuals. These effects have not been shown for female homosexuality, indicating that these two phenomena may have very different origins and dynamics.

Male homosexuality is difficult to explain under Darwinian evolutionary models, because carriers of genes predisposing towards male homosexuality would be likely to reproduce less than average, suggesting that alleles influencing homosexuality should progressively disappear from a population. This changed when previous work by Camperio Ciani and collaborators, published in 2004, showed that females in the maternal line of male homosexuals were more fertile than average.

Challenged by all these empirical data, the authors of the new study published in PLoS ONE considered a range of different hypotheses for the genetic diffusion of male homosexuality. These included: the genetic maternal effects on sons, the heterozygote advantage (as is found in malaria resistance), and “sexually antagonistic selection.” The latter is a particular aspect of Darwinian evolution, in which genetic factors spread in the population by giving a reproductive advantage to one sex while disadvantaging the other. This type of evolution has been previously found in insects, birds, and some mammals, but never in humans.

To discover and clarify the dynamics of the genetic factors for homosexuality, the researchers had to screen a large set of models and exclude them one by one. They concluded that the only possible model was that of sexually antagonistic selection. The other models did not fit the empirical data, either implying that the alleles would become extinct too easily or invade the population, or failing to describe the distribution patterns of male homosexuality and female fecundity observed in the families of homosexuals. Only the model of sexually antagonistic selection involving at least two genes – at least one of which must be on the X chromosome (inherited in males only through their mother) – accounted for all the known data.

The results of this model show the interaction of male homosexuality with increased female fecundity within human populations, in a complex dynamic, resulting in the maintenance of male homosexuality at stable and relatively low frequencies, and highlighting the effects of heredity through the maternal line.

These findings provide new insights into male homosexuality in humans. In particular, they promote a focus shift in which homosexuality should not be viewed as a detrimental trait (due to the reduced male fecundity it entails), but, rather, should be considered within the wider evolutionary framework of a characteristic with gender-specific benefits, and which promotes female fecundity. This may well be the evolutionary origin of this genetic trait in human beings.

The possible widespread occurrence of sexually antagonistic characteristics in evolutionary processes, which play their evolutionary game by giving a fecundity benefit to one sex while disadvantaging the other, has only recently begun to be appreciated. This is understood as a key mechanism through which high levels of genetic variation are maintained in biological populations. Male homosexuality is just the first example of an unknown number of sexually antagonistic traits, which contribute to the maintenance of the natural genetic variability of humans. The new perspectives opened by the models developed for sexually antagonistic selection may also contribute to a better understanding of most genetically-based sexual conflicts, which are, at present, poorly understood in humans.

An unexpected implication of the new models concerns the impact that the sexually antagonistic genetic factors for male homosexuality have on the overall fecundity of a population. The findings suggest that the proportion of male homosexuals may signal a corresponding proportion of females with higher fecundity. Consequently, these factors always contribute, all else being equal, a positive net increase of the fecundity of the whole population, when compared to populations in which such factors are lower or absent. This increase grows as the population baseline fecundity decreases; this means that the genes influencing male homosexuality end up playing the role of a buffer effect on any external factors lowering the overall fecundity of the whole population.

Source: Public Library of Science

Camperio Ciani A, Cermelli P, Zanzotto G (2008) Sexually Antagonistic Selection in Human Male Homosexuality. PLoS ONE 3(6): e2282. doi:10.1371/journal.pone.0002282

Josh says:

Wow. While they did not actually find a gene mutation linked to this, the data fits the model. Certainly it provides an explanation, and I personally like it better than many other explanations. However, whether a male is homosexual or heterosexual cannot be solely genetic, but rather is more likely a genetic predisposition (though I could be wrong). So what about this type of mutation would create such a predisposition?

Note: For those not familiar with the term, fecundity refers to how fertile a female is or how many offspring are produced.

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7 Comments

  1. Andrew Yates said,
    June 18, 2008 @ 12:53 am

    I like how homosexuality is threatening to Darwinian evolutionary models, but traits conducive to civilization: education, wealth, and intelligence, aren’t considered threatening despite an obvious inverse correlation with reproductive success.

    Oh liberal academic politics. Why do you try so hard to rationalize the gays?

  2. Josh Hill said,
    June 18, 2008 @ 1:01 am

    Well, it’s only somewaht recently that wealthier and more educated people had fewer children. Especially in Asian countries, the upper classes had more children. Modern societies are really relatively recent on the human timeline, and such a slight variation in reproduction won’t make much of a difference in that short of period. Also, education and wealth aren’t really tied to genetics; particularly in the United States, many people who are now wealthy had grandparents that were poor and uneducated. The opposite is also true.

  3. Steve said,
    June 18, 2008 @ 4:50 pm

    “I like how homosexuality is threatening to Darwinian evolutionary models, but traits conducive to civilization: education, wealth, and intelligence, aren’t considered threatening despite an obvious inverse correlation with reproductive success.”

    Yeah because dumber animals are less likely to do something stupid that gets them killed. People with wealth are more likely to run out of resources and die and educated people are less likely to be able to build up resources and rear a family. You are obviously horribly blinded by your own agenda and know nothing about evolutionary process. Having fewer offspring does not necessarily mean your reproductive success is worse if they are healthier, happier and have more resources they are more likely to survive.

  4. Andrew Yates said,
    June 18, 2008 @ 6:43 pm

    Steve,

    Better educated, more socially productive people have fewer children later (if any). The survival of children, while applicable to other species and perhaps in human ancient history, is no longer relevant in modern civilization.

    My original tongue-in-cheek comment is because:

    1) Evolution isn’t a perfect system, and “less reproductively fit” organisms can be and are sometimes successful, sometimes for reasons entirely unrelated to fitness. (for example, natural disasters or ordinary chance) There is no “objective” in evolution, and while “fitness” affects the probabilities of what traits will be perpetuated, it’s not a goal nor an axiom.

    2) Sometimes, traits aren’t selectable because biological systems are extremely complex. In this study, the suggestion was that female fecundity and male homosexuality are genetically linked, but it’s possible that homosexuality is simply an emergent attribute of a complex, chaotic biological system.

    3) The “gay gene” gets special research attention because it’s a sensitive political issue, and that amuses me.

  5. Brian said,
    June 18, 2008 @ 9:10 pm

    Andrew and Steve, while there may be a difference in the number of children produced by wealthy and poor people, just because you produce fewer children doesn’t mean you are less fit. Ultimately it is about how many grandchildren you produce. Poor people may have more children, but those children are also more likely to die for many different reason (hunger, malnutrition, increased likelihood of disease, etc.). So the likely hood that poor children survive to reproduce is much smaller compared to rich children who are almost guaranteed a chance to survive to reproduce.

    Traits aren’t selectable? I am not sure what that means. There may be traits which aren’t selected upon because they have no reproductive value, but that doesn’t mean that they aren’t correlated with other traits, nor does it mean that it can’t be selected on in the future. The reason why homosexuality is so interesting biologically is because being gay is an evolutionary dead end. Gay men can’t reproduce if they are exclusively homosexual. If the genes that contribute to homosexuality don’t get passed on, they are selected against using purely evolutionary mechanisms. Yet we still see it in human populations.

    The problem is not with the science. The problem is with reporters and the general public who are trying to use value systems to interpret scienctific evidence and arguments. Saying homosexuality is purely a result of a choatic system is naive and probably more dangerous than saying there is a genetic component to homosexuality. Reporters and the general public who are using a value system to interpret the scientific results are more likely to do harm with “choatic systems” than with “genetic homosexuality” in their writings. Science isn’t supposed to be interpreted with a value system.

  6. Andrew Yates said,
    June 18, 2008 @ 11:28 pm

    > Poor people may have more children, but those children are also more likely to die for many different reason (hunger, malnutrition, increased likelihood of disease, etc.). So the likely hood that poor children survive to reproduce is much smaller compared to rich children who are almost guaranteed a chance to survive to reproduce.

    Not relevant until well after reproductive years virtually everywhere.

    > Gay men can’t reproduce if they are exclusively homosexual. If the genes that contribute to homosexuality don’t get passed on, they are selected against using purely evolutionary mechanisms. Yet we still see it in human populations.

    Neither can the celibate, yet we still have priests and Unix gurus.

    > The problem is not with the science. The problem is with reporters and the general public who are trying to use value systems to interpret scienctific evidence and arguments.

    Yes.

  7. John C said,
    June 19, 2008 @ 12:41 am

    This subject is also addressed in Scientific American Mind, June/July 2008,p68 and it titled: “Bisexual Species”, by Emily Driscoll. Amongst discussion of other animals, the author quotes a researcher in saying that humans should be regarded as bisexual.

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