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Possible Balancing Selection in Human Female Homosexuality

Abstract

A growing number of researchers suggest that female homosexuality is at least in part influenced by genetic factors. Unlike for male homosexuality, few familial studies have attempted to explore maintenance of this apparently fitness-detrimental trait in the population. Using multiple recruitment methods, we explored fecundity and sexual orientation within the pedigrees of 1,458 adult female respondents. We compared 487 homosexual and 163 bisexual with 808 heterosexual females and 30,203 of their relatives. Our data suggest that the direct fitness of homosexual females is four times lower than the direct fitness of heterosexual females of corresponding ages. The prevalence of nonheterosexuality within the homosexual female respondents’ families (2.83%) appear to be more than four times higher than the basal prevalence in the Italian population (0.63%). Pedigree size and relative fecundity in both the paternal and maternal sides of the homosexual women’s families were significantly higher than in the heterosexuals’ families. If confirmed, the relative average fecundity increase within the family seems to offset the loss in fitness due to the low direct fitness of homosexual females. Therefore, the balanced fecundity in the homosexual females’ families may allow the trait to be maintained at a low-frequency equilibrium in the population.

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References

  • Alanko, K., Santtila, P., Harlaar, N., Johansson, K. A., von der Pahlen, B., & Sandnabba, N. K. (2010). Common genetic effects of gender atypical behavior in childhood and sexual orientation in adulthood: a study of finnish twins. Archives of Sexual Behavior, 39, 81–92.

    Article  Google Scholar 

  • Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., et al. (2009). Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychological Science, 20, 144–148.

    Article  Google Scholar 

  • Bailey, J. M., & Bell, A. P. (1993). Familiarity of female and male homosexuality. Behavior Genetics, 23, 313–322.

    Article  Google Scholar 

  • Bailey, J. M., & Benishay, D. S. (1993). Familial aggregation of female sexual orientation. American Journal of Psychiatry, 150, 272–277.

    Article  Google Scholar 

  • Bailey, J. M., & Pillard, R. C. (1991). A genetic study of male sexual orientation. Archives of General Psychiatry, 48, 1089–1096.

    Article  Google Scholar 

  • Bailey, J. M., & Zucker, K. J. (1995). Childhood sex typed behavior and sexual orientation: a conceptual analysis and quantitative review. Developmental Psychology, 31, 43–56.

    Article  Google Scholar 

  • Bailey, J. M., Pillard, R. C., Neale, M. C., & Agyei, Y. (1993). Heritable factors influence sexual orientation in women. Archives of General Psychiatry, 50, 217–223.

    Article  Google Scholar 

  • Bailey, J. M., Dunne, M. P., & Martin, N. G. (2000). Genetic and environmental influences on sexual orientation and its correlates in an Australian twin sample. Journal of Personality and Social Psychology, 78(3), 524–536.

    Article  Google Scholar 

  • Barbagli, M., & Colombo, A. (2007). Omosessuali moderni. Gay e lesbiche in Italia. Bologna: Il Mulino.

    Google Scholar 

  • Barthes, J., Godelle, B., & Raymond, M. (2013). Human social stratification and hypergyny: toward an understanding of male homosexual preference. Evolution and Human Behavior, 34(3), 155–163.

    Article  Google Scholar 

  • Baumeister, R. F. (2000). Gender differences in erotic plasticity: the female sex drive as socially flexible and responsive. Psychological Bulletin, 126, 347–374.

    Article  Google Scholar 

  • Blanchard, R. (2001). Fraternal birth order and the maternal immune hypothesis of male homosexuality. Hormones and Behavior, 40(2), 105–114.

    Article  Google Scholar 

  • Blanchard, R. (2004). Quantitative and theoretical analyses of the relation between older brothers and homosexuality in men. Journal of Theoretical Biology, 230(2), 173–187.

    Article  Google Scholar 

  • Blanchard, R. (2012). Fertility in the mothers of firstborn homosexual and heterosexual men. Archives of Sexual Behavior, 41, 551–556.

    Article  Google Scholar 

  • Blanchard, R., & Klassen, P. (1997). HY antigen and homosexuality in men. Journal of Theoretical Biology, 185(3), 373–378.

    Article  Google Scholar 

  • Blumstein, P. W., & Schwartz, P. (1977). Bisexuality: some social psychological issues. Journal of Social Issues, 33, 30–45.

    Article  Google Scholar 

  • Bogaert, A. (2004). The prevalence of male homosexuality: the effect of fraternal birth order and variations in family size. Journal of Theoretical Biology, 230, 733–770.

    Article  Google Scholar 

  • Burri, A., Cherkas, L., Spector, T., & Rahman, Q. (2011). Genetic and environmental influences on female sexual orientation, childhood gender typicality and adult gender identity. PLoS One, 6(7), e21982.

    Article  Google Scholar 

  • Butler, A. C. (2005). Gender differences in the prevalence of same-sex sexual partnering: 1988–2002. Social Forces, 84, 421–449.

    Article  Google Scholar 

  • Camperio Ciani, A., & Battaglia, U. (2014). Implicit measurements of sexual preference in self-declared heterosexual men: a pilot study on the rate of androphilia in Italy. Journal of Sexual Medicine, 11, 2207–2217.

    Article  Google Scholar 

  • Camperio Ciani, A., & Pellizzari, E. (2012). Fecundity of paternal and maternal nonparental female relatives of homosexual and heterosexual men. PLoS One, 7(12), e51088.

    Article  Google Scholar 

  • Camperio Ciani, A., Corna, F., & Capiluppi, C. (2004). Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity. Proceedings of Royal Society, London B, 271, 2217–2221.

    Article  Google Scholar 

  • Camperio Ciani, A., Cermelli, P., & Zanzotto, G. (2008). Sexually antagonistic selection in human male homosexuality. PLoS One, 3(6), e2282.

    Article  Google Scholar 

  • Camperio Ciani, A., Iemmola, F., & Blecher, S. (2009). Bisexuals and not exclusive homosexuals show evidence of the same genetic factors that promote a female fecundity increase on the maternal line. Journal of Sexual Medicine, 6, 449–455.

    Article  Google Scholar 

  • Camperio Ciani, A., Fontanesi, L., Iemmola, F., Giannella, E., & Ferron, C. (2012). Factors associated with higher fecundity in female maternal relatives of homosexual men. Journal of Sexual Medicine, 9, 2878–2887.

    Article  Google Scholar 

  • Camperio Ciani, A., Battaglia, U., & Zanzotto, G. (2015). Human homosexuality: a paradigmatic arena for sexually antagonistic selection? Cold Spring Harbor Perspectives in Biology, 7(4), a017657.

    Article  Google Scholar 

  • Clinard, M. B., & Meier, R. F. (1979). Sociology of deviant behavior. New York: Holt, Rinehart and Winston.

    Google Scholar 

  • Cloninger, C. R., & Guze, S. B. (1970). Psychiatric illness and female criminality: The role of sociopathy and hysteria in the antisocial woman. American Journal of Psychiatry, 127, 303–311.

    Article  Google Scholar 

  • Cloninger, C. R., & Guze, S. B. (1973). Psychiatric illnesses in the families of female criminals: a study of 288 first-degree relatives. British Journal of Psychiatry, 122, 697–703.

    Article  Google Scholar 

  • Crompton, L. (2006). Homosexuality and civilization. Boston: Harvard University Press.

    Google Scholar 

  • Diamond, M. (1993). Homosexuality and bisexuality in different populations. Archives of Sexual Behavior, 22, 291–310.

    Article  Google Scholar 

  • Diamond, L. M. (2008). Female bisexuality from adolescence to adulthood: results from a 10-year longitudinal study. Developmental Psychology, 44, 5–14.

    Article  Google Scholar 

  • Farr, R. H., & Patterson, C. J. (2013). Coparenting among lesbian, gay, and heterosexual couples: associations with adopted children's outcomes. Child Development, 84(4), 1226–1240.

    Article  Google Scholar 

  • Gavrilets, S., & Rice, W. R. (2006). Genetic models of homosexuality: generating testable predictions. Proceedings of Royal Society, London B, 273, 3031–3038.

    Article  Google Scholar 

  • Hamer, D. H., Hu, S., Magnuson, V. L., Hu, N., & Pattatucci, A. M. (1993). A linkage between DNA markers on the X-chromosome and male sexual orientation. Science, 261, 321–327.

    Article  Google Scholar 

  • Hamilton, W. D. (1963). The evolution of altruistic behavior. American Naturalist, 97, 354–356.

    Article  Google Scholar 

  • Heckathorn, D. D. (1997). Respondent-driven sampling a new approach to the study of hidden populations. Social Problems, 44, 174–199.

    Article  Google Scholar 

  • Herdt, G. H. (1997). Same sex, different cultures: gays and homosexual females across cultures. Boulder: Westview Press.

    Google Scholar 

  • Hershberger, S. L., Pilkington, N. W., & D’Augelli, A. R. (1997). Predictors of suicide attempts among gay, lesbian, and bisexual youth. Journal of Adolescent Research, 12(4), 477–497.

    Article  Google Scholar 

  • Hines, M., Golombok, S., Rust, J., Johnston, K. J., Golding, J., & the Avon Longitudinal Study of Parents and Children Study Team. (2002). Testosterone during pregnancy and gender role behavior of preschool children: a longitudinal, population study. Child Development, 73, 1678–1687.

    Article  Google Scholar 

  • Hines, M., Brook, C., & Conway, G. S. (2004). Androgen and psychosexual development: core gender identity, sexual orientation and recalled childhood gender role behavior in women and men with congenital adrenal hyperplasia (CAH). Journal of Sex Research, 41, 75–81.

    Article  Google Scholar 

  • Hoskins, J. L., Ritchie, M. G., & Bailey, N. W. (2015). A test of genetic models for the evolutionary maintenance of same-sex sexual behaviour. Proceedings of the Royal Society B., 282(1809), 20150429.

    Article  Google Scholar 

  • Hu, S., Pattatucci, A. M., Patterson, C., Li, L., Fulker, D. W., Cherny, S. S., et al. (1995). Linkage between sexual orientation and chromosome Xq28 in males but not in females. Nature Genetics, 11, 248–256.

    Article  Google Scholar 

  • Iemmola, F., & Camperio Ciani, A. (2009). New evidence of genetic factors influencing sexual orientation in men: female fecundity increase in the maternal line. Archives of Sexual Behavior, 38, 393–399.

    Article  Google Scholar 

  • Jannini, E. A., Blanchard, R., Camperio Ciani, A., & Bancroft, J. (2010). Male homosexuality: Nature or culture? Journal of Sexual Medicine, 7, 3245–3253.

    Article  Google Scholar 

  • Johnson, C. J. (1997). Congenital adrenal hyperplasia and adult sexual behavior. Journal of the American Medical Association, 278, 549.

    Article  Google Scholar 

  • Kendler, K. S., Thornton, L. M., Gilman, S. E., & Kessler, R. C. (2000). Sexual orientation in a US national sample of twin and nontwin sibling pairs. American Journal of Psychiatry, 157, 1843–1846.

    Article  Google Scholar 

  • King, M., Green, J., Osborn, D. P. J., Arkell, J., Hetherton, J., & Pereira, E. (2005). Family size in white gay and heterosexual men. Archives of Sexual Behavior, 34, 117–122.

    Article  Google Scholar 

  • Kinsey, A. C., Martin, C. E., & Pomeroy, W. B. (1948). Sexual behavior in the human male. Philadelphia: Saunders.

    Google Scholar 

  • Kinsey, A., Pomeroy, W., Martin, C. E., & Gebhard, P. (1953). Sexual behavior in the human female. Philadelphia: Saunders.

    Google Scholar 

  • Kirk, K. M., Bailey, J. M., & Martin, N. G. (1999). How accurate is the family history method for assessing siblings' sexual orientation? Archives of Sexual Behavior, 28, 129–137.

    Article  Google Scholar 

  • Långström, N., Rahman, Q., Carlström, E., & Lichtenstein, P. (2010). Genetic and environmental effects on same-sex sexual behavior: A population study of twins in Sweden. Archives of Sexual Behavior, 39, 75–80.

    Article  Google Scholar 

  • Lippa, R. A. (2006). Finger lengths, 2D: 4D ratios, and their relation to gender-related personality traits and the big five. Biological Psychology, 71, 116–121.

    Article  Google Scholar 

  • Maynard Smith, J. (1998). Evolutionary genetics (2nd ed.). Oxford: Oxford University Press.

    Google Scholar 

  • Meyer-Bahlburg, H. F., Dolezal, C., Baker, S. W., & New, M. I. (2008). Sexual orientation in women with classical or nonclassical congenital adrenal hyperplasia as a function of degree of prenatal androgen excess. Archives of Sexual Behavior, 37, 85–99.

    Article  Google Scholar 

  • Mondimore, F. M. (1996). A natural history of homosexuality. Baltimore: Johns Hopkins University Press.

    Google Scholar 

  • Moran, P. A. P. (1972). Familial effects in schizophrenia and homosexuality. Australian and New Zealand Journal of Psychiatry, 6, 116–119.

    Article  Google Scholar 

  • Nash, G. (2001). The subversive male: homosexual and bestial images on european mesolithic rock art. In L. Bevan (Ed.), Indecent exposure: sexuality, society and the archaeological record (pp. 43–55). Glasgow: Cruithne Press.

    Google Scholar 

  • Pacilli, M. G., Taurino, A., Jost, J. T., & van der Toorn, J. (2011). System justification, right-wing conservatism, and internalized homophobia: Gay and homosexual female attitudes toward same-sex parenting in Italy. Sex Roles, 65, 580–595.

    Article  Google Scholar 

  • Pattatucci, A. M. L. (1998). Molecular investigations into complex behavior: lessons from sexual orientation studies. Human Biology., 70, 367–386.

    Google Scholar 

  • Pattatucci, A. M. L., & Hamer, D. H. (1995). Development and familiality of sexual orientation in females. Behavior Genetics, 25, 407–419.

    Article  Google Scholar 

  • Patterson, C. J., & Riskind, R. G. (2010). To be a parent: issues in family formation among gay and lesbian adults. Journal of GLBT Family Studies, 6, 326–340.

    Article  Google Scholar 

  • Pillard, R. C., & Weinrich, J. D. (1986). Evidence of familial nature of male homosexuality. Archives of General Psychiatry, 43(8), 808–812.

    Article  Google Scholar 

  • Pillard, R. C., Poumadere, J., & Carretta, R. A. (1981). Is homosexuality familial? A review, some data, and a suggestion. Archives of Sexual Behavior, 10, 465–475.

    Article  Google Scholar 

  • Plomin, R., DeFries, J. C., McClearn, G. E., & McGuffin, P. (2001). Behavioral genetics (4th ed.). New York: Worth.

    Google Scholar 

  • Posthuma, D., Beem, A. L., de Geus, E. J. C., van Baal, G. M., von Hjelmborg, J. B., Iachine, I., et al. (2003). Theory and practice in quantitative genetics. Twin Research, 6, 361–376.

    Article  Google Scholar 

  • Rahman, Q. (2005). The neurodevelopment of human sexual orientation. Neuroscience and Biobehavioral Reviews, 29, 1057–1066.

    Article  Google Scholar 

  • Rieger, G., Blanchard, R., Schwartz, G., Bailey, J. M., & Sanders, A. R. (2012). Further data concerning Blanchard’s (2011) “Fertility in the mothers of firstborn homosexual and heterosexual men”. Archives of Sexual Behavior, 41, 529–531.

    Article  Google Scholar 

  • Rosenbluth, S. (1997). Is sexual orientation a matter of choice? Psychology of Women Quarterly, 21, 595–610.

    Article  Google Scholar 

  • Rust, P. C. (1992). The politics of sexual identity: sexual attraction and behavior among lesbian and bisexual women. Social Problems, 39(4), 366–386.

    Article  Google Scholar 

  • Sanders, A. R., Martin, E. R., Beecham, G. W., Guo, S., Dawood, K., et al. (2015). Genome-wide scan demonstrates significant linkage for male sexual orientation. Psychological Medicine, 45, 1379–1388.

    Article  Google Scholar 

  • Savin-Williams, R. C. (2006). Who's gay? Does it matter? Current Directions in Psychological Science, 15, 40–44.

    Article  Google Scholar 

  • Schur, E. (1965). Crimes without victims. Englewood Cliffs: Prentice-Hall.

    Google Scholar 

  • Sell, R. L., Wells, J. A., & Wypij, D. (1995). The prevalence of homosexual behavior and attraction in the United States, the United Kingdom and France: Results of national population-based samples. Archives of Sexual Behavior, 24, 235–248.

    Article  Google Scholar 

  • Spitzer, R. L. (1981). The diagnostic status of homosexuality in DSM-III: a reformulation of the issues. American Journal of Psychiatry, 138(2), 210–215.

    Article  Google Scholar 

  • Spreen, M. (1992). Rare populations, hidden populations, and link-tracing designs: what and why? Bulletin de Methodologie Sociologique, 36, 34–58.

    Article  Google Scholar 

  • Stein, T. S. (1997). Deconstructing sexual orientation: understanding the phenomena of sexual orientation. Journal of Homosexuality, 34, 81–86.

    Article  Google Scholar 

  • Stout, S. A., Litvak, M., Robbins, N. M., & Sandberg, D. E. (2010). Congenital adrenal hyperplasia: classification of studies employing psychological endpoints. International Journal of Pediatric Endocrinology. https://doi.org/10.1155/2010/191520.

  • Tafuri, S., Martinelli, D., Germinario, C., & Prato, R. A. (2011). Study on the sexual and contraception behaviours of the pre-university students in Puglia (South-Italy). Journal of Preventive Medicine and Hygiene, 52, 219–223.

    Google Scholar 

  • Taylor, M., & Abrams, R. (1973). Manic states. A genetic study of early and late onset affective disorders. Archives of General Psychiatry, 28, 656–658.

    Article  Google Scholar 

  • VanderLaan, D. P., Forrester, D. L., Petterson, L. J., & Vasey, P. L. (2012). Offspring production among the extended relatives of Samoan men and fa'afafine. PLoS One, 7(4), e36088.

    Article  Google Scholar 

  • VanderLaan, D. P., Garfield, Z. H., Garfield, M. J., Leca, J.-B., Vasey, P. L., & Hames, R. B. (2014). The “female fertility–social stratification–hypergyny” hypothesis of male homosexual preference: factual, conceptual and methodological errors in Barthes et al. [commentary]. Evolution and Human Behavior, 35(5), 445–447.

    Article  Google Scholar 

  • Vasey, P. L., & VanderLaan, D. P. (2010). Avuncular tendencies and the evolution of male androphilia in Samoan fa’afafine. Archives of Sexual Behavior, 39(4), 821–830.

    Article  Google Scholar 

  • Vasey, P. L., Pocock, D. S., & VanderLaan, D. P. (2007). Kin selection and male androphilia in Samoan fa'afafine. Evolution and Human Behavior, 28(3), 159–167.

    Article  Google Scholar 

  • Watters, J. K., & Biernacki, P. (1989). Targeted sampling: options for the study of hidden populations. Social Problems, 36, 416–430.

    Article  Google Scholar 

  • Whisman, V. (1996). Queer by choice: lesbians, gay men and the politics of identity. New York: Routledge.

    Google Scholar 

  • Wilson, S. (2004). Gay, lesbian, bisexual and transgender identification and attitudes to same-sex relationships in Australia and the United States. People and Place, 12(4), 12–21.

    Google Scholar 

  • Wright, J. ed. (2009). Homosexuality in the U.S., 1998–2000. In The New York Times almanac (p. 314). New York: Penguin Reference.

  • Zucker, K. J., Bradley, S. J., Oliver, G., Blake, J., Fleming, S., et al. (1996). Psychosexual development of women with congenital adrenal hyperplasia. Hormones and Behavior, 30, 300–318.

    Article  Google Scholar 

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Acknowledgements

This research was partly funded by a BIRD 2017 research grant from the University of Padova, Italy, assigned to Andrea Camperio Ciani.

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Camperio Ciani, A., Battaglia, U., Cesare, L. et al. Possible Balancing Selection in Human Female Homosexuality. Hum Nat 29, 14–32 (2018). https://doi.org/10.1007/s12110-017-9309-8

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Keywords

  • Female homosexuality
  • Fecundity
  • Fitness
  • Pedigrees
  • Balancing selection