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An alternative hypothesis for the evolution of same-sex sexual behaviour in animals

Nature Ecology & Evolution volume 3, pages 1622–1631 (2019)Cite this article

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Matters Arising to this article was published on 20 April 2020

Matters Arising to this article was published on 20 April 2020

An Author Correction to this article was published on 25 November 2019

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Abstract

Same-sex sexual behaviour (SSB) has been recorded in over 1,500 animal species with a widespread distribution across most major clades. Evolutionary biologists have long sought to uncover the adaptive origins of ‘homosexual behaviour’ in an attempt to resolve this apparent Darwinian paradox: how has SSB repeatedly evolved and persisted despite its presumed fitness costs? This question implicitly assumes that ‘heterosexual’ or exclusive different-sex sexual behaviour (DSB) is the baseline condition for animals, from which SSB has evolved. We question the idea that SSB necessarily presents an evolutionary conundrum, and suggest that the literature includes unchecked assumptions regarding the costs, benefits and origins of SSB. Instead, we offer an alternative null hypothesis for the evolutionary origin of SSB that, through a subtle shift in perspective, moves away from the expectation that the origin and maintenance of SSB is a problem in need of a solution. We argue that the frequently implicit assumption of DSB as ancestral has not been rigorously examined, and instead hypothesize an ancestral condition of indiscriminate sexual behaviours directed towards all sexes. By shifting the lens through which we study animal sexual behaviour, we can more fruitfully examine the evolutionary history of diverse sexual strategies.

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Fig. 1: Examples of species with documented SSB demonstrate the widespread distribution of SSB in animals.

a, Leo Francini/Alamy Stock Photo; b, reproduced from ref. 87, © 2016 Norimasa Sugita under a Creative Commons licence CC BY 4.0; c, blickwinkel/Alamy Stock Photo; d, NOAA (https://oceanexplorer.noaa.gov/explorations/06davidson/logs/summary/media/squid_600.html); e, © Aaron Goodwin; f, robertharding/Alamy Stock Photo; g, Alex Fieldhouse/Alamy Stock Photo; h, Frans Lanting Studio/Alamy Stock Photo; i, Photo by Peggy Greb, USDA Agricultural Research Service; j, Gerald McCormack; k, pxhere under a Creative Commons licence CCO 1.0; l, reproduced from ref. 40, Springer; m, Brian Jeffery Beggerly under a Creative Commons licence CC BY 2.0; n, National Geographic Image Collection/Alamy Stock Photo; o, Arterra Picture Library/Alamy Stock Photo; p, reproduced from ref. 98, © 2013 Nieuwenhuizen et al. under a Creative Commons licence CC BY 4.0; q, blickwinkel/Alamy Stock Photo; r, Hal Beral/VWPics/Alamy Stock Photo

Fig. 2: Conceptual representation of the variation in SSB and DSB that is possible at the individual and population, and species levels.
Fig. 3: Ecological, evolutionary and developmental factors may influence the expression of SSB.

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Acknowledgements

This project could not have come to fruition without many dynamic and thought-provoking conversations with natural and social scientists, feminists, LGBTQIA+ activists, friends and family members. We particularly thank A. Wesner and the members of the Queer Ecologies Working Group within the Social Science Matrix at UC Berkeley, who facilitated a workshop and public discussion of a draft of this manuscript which proved instrumental to our thinking. S. Pitnick and the members of the Center for Reproductive Evolution at Syracuse University also provided valuable comments on an earlier draft. We also thank P. Muralidhar, Y. Stuart, E. Burnell and A. Roddy for their feedback and ideas as we discussed this project. E. Milam provided a key grounding in history of science, and we direct all readers to her important body of work. We benefited greatly from participating in ongoing online and in-person discussions regarding gender, sexuality and the history of science, including engaging with the excellent Project Biodiversify (projectbiodiversify.org) and at the Evolution 2019 conference. J.D.M. was supported by a Dean’s Emerging Scholars Fellowship from Yale University, A.K. was supported by the Miller Institute for Basic Research in Science at UC Berkeley, M.R.L. was supported by the National Science Foundation and the David H. Smith Fellowship, and C.E.M. was supported by a Graduate Research Fellowship from the National Science Foundation and a Scholar Award from the Philanthropic Educational Organization. Figures were designed with Andrew Benson (https://benson.graphics/).

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Authors and Affiliations

  1. School of Forestry and Environmental Studies, Yale University, New Haven, CT, USA

    Julia D. Monk

  2. Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA

    Erin Giglio

  3. Miller Institute for Basic Research in Science, University of California Berkeley, Berkeley, CA, USA

    Ambika Kamath

  4. Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, USA

    Ambika Kamath & Max R. Lambert

  5. Center for Reproductive Evolution, Department of Biology, Syracuse University, Syracuse, NY, USA

    Caitlin E. McDonough

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All authors contributed equally to the manuscript and share first authorship, with authors listed alphabetically after the corresponding author. J.D.M. and M.R.L. conceived of the paper. E.G., A.K. and C.E.M. developed the concepts substantially, and all authors wrote and revised the manuscript.

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Monk, J.D., Giglio, E., Kamath, A. et al. An alternative hypothesis for the evolution of same-sex sexual behaviour in animals. Nat Ecol Evol 3, 1622–1631 (2019). https://doi.org/10.1038/s41559-019-1019-7

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