Skip to main content
Log in

De-Scent with Modification: More Evidence and Caution Needed to Assess Whether the Loss of a Pheromone Signaling Protein Permitted the Evolution of Same-Sex Sexual Behavior in Primates

  • Commentary
  • Published:
Archives of Sexual Behavior Aims and scope Submit manuscript

The Original Article was published on 23 April 2019

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Aujard, F. (1997). Effect of vomeronasal organ removal on male socio-sexual responses to female in a prosimian primate (Microcebus murinus). Physiology & Behavior, 62(5), 1003–1008.

    Article  Google Scholar 

  • Bailey, N. W., & Zuk, M. (2009). Same-sex sexual behavior and evolution. Trends in Ecology & Evolution, 24(8), 439–446.

    Article  Google Scholar 

  • Baxi, K. N., Dorries, K. M., & Eisthen, H. L. (2006). Is the vomeronasal system really specialized for detecting pheromones? Trends in Neurosciences, 29, 1–7. https://doi.org/10.1016/j.tins.2005.10.002.

    Article  PubMed  Google Scholar 

  • Bezanson, M., & McNamara, A. (2019). The what and where of primate field research may be failing primate conservation. Evolutionary Anthropology, 28(4), 166–178.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolnick, D. A., Smith, R. W. A., & Fuentes, A. (2019). Vital topics forum: How academic diversity is transforming scientific knowledge in biological anthropology. American Anthropologist, 121, 464. https://doi.org/10.1111/aman.13212.

    Article  Google Scholar 

  • Borowsky, B., Adham, N., Jones, K. A., Raddatz, R., Artymyshyn, R., Ogozalek, K. L., … Gerald, C. (2001). Trace amines: Identification of a family of mammalian G protein-coupled receptors. Proceedings of the National Academy of Sciences, 98(16), 8966–8971.

    Article  Google Scholar 

  • Bravmann, S. (1997). Queer fictions of the past: History, culture, and difference. Cambridge, MA: Cambridge University Press.

    Google Scholar 

  • Bunzow, J. R., Sonders, M. S., Arttamangkul, S., Harrison, L. M., Zhang, G., Quigley, D. I., … Grandy, D. K. (2001). Amphetamine, 3, 4-methylenedioxymethamphetamine, lysergic acid diethylamide, and metabolites of the catecholamine neurotransmitters are agonists of a rat trace amine receptor. Molecular Pharmacology, 60(6), 1181–1188.

    Article  PubMed  Google Scholar 

  • Busia, L., Denice, A. R., Aureli, F., & Schaffner, C. M. (2018). Homosexual behavior between male spider monkeys (Ateles geoffroyi). Archives of Sexual Behavior, 47(4), 857–861.

    Article  PubMed  Google Scholar 

  • Candolin, U. (2003). The use of multiple cues in mate choice. Biological Reviews, 78(4), 575–595.

    Article  PubMed  Google Scholar 

  • Conkey, M. W., & Spector, J. D. (1984). Archaeology and the study of gender. Advances in the Study of Archaeological Method and Theory, 7, 1–32.

    Google Scholar 

  • Diamond, L. M., & Rosky, C. J. (2016). Scrutinizing immutability: Research on sexual orientation and U.S. legal advocacy for sexual minorities. Journal of Sex Research, 53(4–5), 363–391.

    Article  PubMed  Google Scholar 

  • Dixson, A. F. (1983). Observations on the evolution and behavioral significance of “sexual skin” in female primates. Advances in the Study of Behavior, 13, 63–106.

    Article  Google Scholar 

  • Drea, C. M. (2015). D’scent of man: A comparative survey of primate chemosignaling in relation to sex. Hormones and Behavior, 68, 117–133.

    Article  PubMed  Google Scholar 

  • Duberman, M. B. (1988). Reclaiming the gay past. Reviews in American History, 16(4), 515–525.

    Article  Google Scholar 

  • Eizirik, R., Murphy, W. J., & O’Brien, S. J. (2001). Molecular dating and biogeography of the early placental mammal radiation. Journal of Heredity, 92(2), 212–219.

    Article  PubMed  Google Scholar 

  • Epple, G. (1980). Relationships between aggression, scent-marking and gonadal state in a primate, the tamarin, Saguinus fuscicollis. In D. Muller-Schwarze & R. M. Silverstein (Eds.), Chemical signals, vertebrates and aquatic invertebrates (pp. 87–105). New York: Plenum Press.

    Chapter  Google Scholar 

  • Fernandez-Duque, E., Mason, W. A., & Mendoza, S. (1997). Effects of duration of separation on responses to mates and strangers in the monogamous titi monkey (Callicebus moloch). American Journal of Primatology, 43(3), 225–237.

    Article  PubMed  Google Scholar 

  • Ford, S. M. (1994). Evolution of sexual dimorphism in body weight in platyrrhines. American Journal of Primatology, 34(2), 221–244.

    Article  PubMed  Google Scholar 

  • Fortes-Marco, L., Lanuza, E., & Martinez-Garcia, F. (2013). Of pheromones and kairomones: What receptors mediate innate emotional response. Anatomical Record, 296(9), 1346–1363.

    Article  Google Scholar 

  • Fout, J. C. (1992). Sexual politics in Wilhelmine Germany: The male gender crisis, moral purity, and homophobia. Journal of the History of Sexuality, 2(3), 388–421.

    PubMed  Google Scholar 

  • Fuentes, A. (2002). Patterns and trends in primate pair bonds. International Journal of Primatology, 23(5), 953–978.

    Article  Google Scholar 

  • Futuyma, D. J., & Risch, S. J. (1984). Sexual orientation, sociobiology, and evolution. Journal of Homosexuality, 9, 157–168.

    Article  Google Scholar 

  • Goldfoot, D. A., Asa, S. M., Essock-Vitale, C. S., Thornton, J. E., & Leshner, A. I. (1978). Anosmia in male rhesus monkeys does not alter copulatory activity with cycling females. Science, 199, 1095–1096.

    Article  PubMed  Google Scholar 

  • Gómez, J. M., Verdú, M., González-Megías, A., & Méndez, M. (2016). The phylogenetic roots of human lethal violence. Nature, 538, 233–237.

    Article  PubMed  Google Scholar 

  • Haldeman, D. C. (1994). The practice and ethics of sexual orientation conversion therapy. Journal of Consulting and Clinical Psychology, 62(2), 221–227.

    Article  PubMed  Google Scholar 

  • Hare, B., Wobber, V., & Wrangham, R. (2012). The self-domestication hypothesis: Evolution of bonobo psychology is due to selection against aggression. Animal Behaviour, 83(3), 573–585.

    Article  Google Scholar 

  • Herrn, R. (1995). On the history of biological theories of homosexuality. Journal of Homosexuality, 28(1–2), 31–56.

    Article  PubMed  Google Scholar 

  • Higham, J. P., Heistermann, M., Saggau, C., Agil, M., Perwitasari-Farajallah, D., & Engelhardt, A. (2012). Sexual signaling in female crested macaques and the evolution of primate fertility signals. BMC Evolutionary Biology, 12, 89. https://doi.org/10.1186/1471-2148-12-89.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hohenbrink, P., Dempewolf, S., Zimmermann, E., Mundy, N. I., & Radespiel, U. (2014). Functional promiscuity in a mammalian chemosensory system: Extensive expression of vomeronasal receptors in the main olfactory epithelium of mouse lemurs. Frontiers in Neuroanatomy, 8, 102. https://doi.org/10.3389/fnana.2014.00102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter, A. J., & Dixson, A. F. (1983). Anosmia and aggression in male owl monkeys (Aotus trivirgatus). Physiology & Behavior, 30(6), 875–879.

    Article  Google Scholar 

  • Jasinska, A. J., Schmitt, C. A., Service, S. K., Cantor, R. M., Dewar, K., Jentsch, D. J., … Freimer, N. B. (2013). Systems biology of the vervet monkey. Institute for Laboratory Animal Research Journal, 54, 122–143.

    Article  Google Scholar 

  • Joel, D. (2012). Genetic-gonadal-genitals sex (3G-sex) and the misconception of brain and gender, or, why 3G-males and 3G-females have intersex brain and intersex gender. Biology of Sex Differences, 3, 1–6. https://doi.org/10.1186/2042-6410-3-27.

    Article  Google Scholar 

  • Joel, D., Tarrasch, R., Berman, Z., Mukamel, M., & Ziv, E. (2014). Queering gender: Studying gender identity in ‘normative’ individuals. Psychology & Sexuality, 5, 291–321.

    Article  Google Scholar 

  • Keller, M., & Lévy, F. (2012). The main but not the accessory olfactory system is involved in the processing of socially relevant chemosignals in ungulates. Frontiers in Neuroanatomy, 6, 39. https://doi.org/10.3389/fnana.2012.00039.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kowalewski, M. M., & Garber, P. A. (2010). Mating promiscuity and reproductive tactics in female black and gold howler monkeys (Alouatta caraya) inhabiting an island on the Parana River, Argentina. American Journal of Primatology, 72(8), 734–748.

    Article  PubMed  Google Scholar 

  • Kratzing, J. (1971). The structure of the vomeronasal organ in the sheep. Journal of Anatomy, 108(Pt 2), 247–260.

    PubMed  PubMed Central  Google Scholar 

  • LeVay, S. (1991). A difference in hypothalamic structure between heterosexual and homosexual men. Science, 253, 1034–1037.

    Article  PubMed  Google Scholar 

  • Liberles, S. D. (2015). Trace amine-associated receptors: Ligands, neural circuits, and behaviors. Current Opinion in Neurobiology, 34, 1–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Manson, J. H., Perry, S., & Parish, A. (1997). Nonconceptive sexual behavior in bonobos and capuchins. International Journal of Primatology, 18(5), 767–786.

    Article  Google Scholar 

  • Meredith, S. M., & Schmitt, C. A. (2019). The outliers are in: Queer perspectives on investigating variation in biological anthropology. American Anthropologist, 121(2), 487–489.

    Article  Google Scholar 

  • Mooallem, J. (2010, March 29). Can animals be gay? New York Times. Retrieved September 22, 2019, from http://www.nytimes.com/2010/04/04/magazine/04animals-t.html?.

  • Moss, I. (2014). Ending reparative therapy in minors: An appropriate legislative response. Family Court Review, 52(2), 316–329.

    Article  Google Scholar 

  • Nidiffer, M. D., & Cortés-Ortíz, L. (2015). Intragroup genetic relatedness in two howler monkey species (Alouatta pigra and A. palliata): Implications for understanding social systems and dispersal. American Journal of Primatology, 77(12), 1333–1345.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohara, H., Nikaido, M., Date-Ito, A., Mogi, K., Okamura, H., Okada, N., … Hagino-Yamagishi, K. (2009). Conserved repertoire of orthologous vomeronasal type 1 receptor genes in ruminant species. BMC Evolutionary Biology, 9, 233. https://doi.org/10.1186/1471-2148-9-233.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira, M. E., & Kappeler, P. M. (1997). Divergent systems of agonistic behavior in Lemurid primates. Behaviour, 134, 225–274.

    Article  Google Scholar 

  • Pfau, D., Jordan, C. L., & Breedlove, S. M. (2019). The de-scent of sexuality: Did loss of a pheromone signaling protein permit the evolution of same-sex sexual behavior in primates? Archives of Sexual Behavior. https://doi.org/10.1007/s10508-018-1377-2.

    Article  PubMed  Google Scholar 

  • Pope, T. R. (2000). Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus). Behavioral Ecology and Sociobiology, 48(4), 253–267.

    Article  Google Scholar 

  • Rigall, L., Higham, J. P., Lee, P. C., Blin, A., & Garcia, C. (2013). Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). American Journal of Primatology, 75(7), 774–787.

    Article  Google Scholar 

  • Rodriguez, I., Greer, C. A., Mok, M. Y., & Mombaerts, P. (2000). A putative pheromone receptor gene expressed in human olfactory mucosa. Nature Genetics, 26(1), 18–19.

    Article  PubMed  Google Scholar 

  • Roselli, C. E., Reddy, R. C., & Kaufman, K. R. (2011). The development of male-oriented behavior in rams. Frontiers in Neuroendocrinology, 32(2), 164–169.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salazar, I., Quinteiro, P. S., Alemañ, N., Cifuentes, J. M., & Troconiz, P. F. (2007). Diversity of the vomeronasal system in mammals: The cingularities of the sheep model. Microscopy Research and Technique, 70(8), 752–762.

    Article  PubMed  Google Scholar 

  • Salazar, I., & Sánchez-Quinteiro, P. (2009). The risk of extrapolation in neuroanatomy: The case of the mammalian vomeronasal system. Frontiers in Neuroanatomy, 3, 22. https://doi.org/10.3389/neuro.05/022.2009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schultz, S., Opie, C., & Atkinson, Q. D. (2011). Stepwise evolution of stable sociality in primates. Nature, 479, 219–222.

    Article  Google Scholar 

  • Sheldon, J. P., Pfeffer, C. A., Epstein Jayarantne, T., Feldbaum, M., & Petty, E. M. (2007). Beliefs about the etiology of homosexuality and about the ramifications of discovering its possible genetic origin. Journal of Homosexuality, 52, 111–150.

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva, L., & Antunes, A. (2017). Vomeronasal receptors in vertebrates and the evolution of pheromone detection. Annual Reviews in Animal Biosciences, 5, 353–370.

    Article  Google Scholar 

  • Sussman, R. W., Garber, P. A., & Cheverud, J. M. (2005). Importance of cooperation and affiliation in the evolution of primate sociality. American Journal of Physical Anthropology, 128(1), 84–97.

    Article  PubMed  Google Scholar 

  • van Anders, S. M. (2015). Beyond sexual orientation: Integrating gender/sex and diverse sexualities via sexual configurations theory. Archives of Sexual Behavior, 44(5), 1177–1213.

    Article  PubMed  Google Scholar 

  • Van Belle, S., Estrada, A., & Di Fiore, A. (2014). Kin-biased spatial associations and social interactions in male and female black howler monkeys (Alouatta pigra). Behaviour, 151, 2029–2057.

    Article  Google Scholar 

  • Van Gossum, H., De Bruyn, L., & Stoks, R. (2005). Reversible switches between male–male and male–female mating behaviour by male damselflies. Biology Letters, 1, 268–270.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasey, P., Chapais, B., & Gauthier, C. (1998). Mounting interactions between female Japanese macaques: Testing the influence of dominance and aggression. Ethology, 104(5), 387–398.

    Article  Google Scholar 

  • Voss, B. L., & Schmidt, R. A. (2000). Archaeologies of sexuality: An introduction. In R. A. Schmidt & B. L. Voss (Eds.), Archaeologies of sexuality (pp. 1–32). London: Routledge.

    Google Scholar 

  • Walters, S. D. (2014). The tolerance trap: How God, genes, and good intentions are sabotaging gay equality. New York: New York University Press.

    Google Scholar 

  • Westphal, C. F. O. (1870). Die conträre sexualempfindung: Symptom eines neuropathischen (psychopathischen) zustandes. Archiv für Psychiatrie und Nervenkrankheiten, 2, 73–108.

    Article  Google Scholar 

  • Wolovich, C. K., Evans, S., & Green, S. M. (2010). Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex difference in response to unfamiliar male and female conspecifics. American Journal of Primatology, 72(11), 942–950.

    Article  PubMed  Google Scholar 

  • Yoder, J. (18 June, 2019). Let the mystery be? Slate. Retrieved September 22, 2019, from https://slate.com/human-interest/2019/06/gay-genetic-research-dna-screening-risks.html.

  • Zuk, M. (2002). Sexual selections: What we can and can’t learn about sex from animals. Berkeley: University of California Press.

    Book  Google Scholar 

Download references

Acknowledgements

We would like to thank Paul Vasey for his invitation to submit this commentary. CAS would like to thank Claudia Astorino, Eliot Chudyk, Cati Connell, Lynn Hallstein O’Brien, Cheryl Knott, Alyssa Kriekemeier, Stephanie Meredith, Roberta Micallef, Takeo Rivera, Rick W. A. Smith, Karen Warkentin, and the students of the Spring 2019 semester of BU’s Women’s, Gender, and Sexuality Studies Program course Gender & Sexuality II, for numerous enjoyable discussions that have informed these perspectives.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher A. Schmitt.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and Animal Rights

This article does not involve novel research with human or non-human subjects requiring ethical clearance.

Informed Consent

Not Applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schmitt, C.A., Garrett, E.C. De-Scent with Modification: More Evidence and Caution Needed to Assess Whether the Loss of a Pheromone Signaling Protein Permitted the Evolution of Same-Sex Sexual Behavior in Primates. Arch Sex Behav 50, 2301–2307 (2021). https://doi.org/10.1007/s10508-019-01583-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10508-019-01583-z

Navigation