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

Article metrics

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

Change history

  • 25 November 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. 1.

    Darwin, C. On The Origin of Species by Means of Natural Selection, or Preservation of Favoured Races in the Struggle for Life (J. Murray, 1859).

  2. 2.

    Darwin, C. The Descent of Man, and Selection in Relation to Sex (J. Murray, 1871).

  3. 3.

    Sommer, V. & Vasey, P. L. Homosexual Behaviour in Animals: An Evolutionary Perspective (Cambridge Univ. Press, 2006).

  4. 4.

    Gunst, N., Vasey, P. L. & Leca, J.-B. Deer mates: a quantitative study of heterospecific sexual behaviors performed by Japanese macaques toward sika deer. Arch. Sex. Behav. 47, 847–856 (2017).

  5. 5.

    Swift, K. & Marzluff, J. M. Occurrence and variability of tactile interactions between wild American crows and dead conspecifics. Philos. Trans. R. Soc. B 373, 20170259 (2018).

  6. 6.

    Gwynne, D. T. & Rentz, D. C. F. Beetles on the bottle: male Buprestids mistake stubbies for females (Coleoptera). Aust. J. Entomol. 22, 79–80 (1983).

  7. 7.

    McDonnell, S. M., Henry, M. & Bristol, F. Spontaneous erection and masturbation in equids. J. Reprod. Fertil. (Suppl.) 44, 664–665 (1991).

  8. 8.

    Bailey, N. W. & Zuk, M. Same-sex sexual behavior and evolution. Trends Ecol. Evol. 24, 439–446 (2009).

  9. 9.

    Terry, J. ‘Unnatural acts’ in nature: the scientific fascination with queer animals. GLQ 6, 151–193 (2000).

  10. 10.

    Roughgarden, J. Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People (Univ. California Press, 2004).

  11. 11.

    Scharf, I. & Martin, O. Y. Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences. Behav. Ecol. Sociobiol. 67, 1719–1730 (2013).

  12. 12.

    Bagemihl, B. Biological Exuberance: Animal Homosexuality and Natural Diversity (Macmillan, 1999).

  13. 13.

    Savolainen, V. & Hodgson, J. A. in Encyclopedia of Evolutionary Psychological Science (eds Weekes-Shackelford, V., Shackelford, T. K. & Weekes-Shackelford, V. A.) 1–8 (Springer, 2016).

  14. 14.

    Gavrilets, S. & Rice, W. R. Genetic models of homosexuality: generating testable predictions. Proc. R. Soc. B 273, 3031–3038 (2006).

  15. 15.

    Berger, D. et al. Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior. BMC Evol. Biol. 16, 88 (2016).

  16. 16.

    Sales, K. et al. Experimental evolution with an insect model reveals that male homosexual behaviour occurs due to inaccurate mate choice. Anim. Behav. 139, 51–59 (2018).

  17. 17.

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

  18. 18.

    Mizumoto, N., Yashiro, T. & Matsuura, K. Male same-sex pairing as an adaptive strategy for future reproduction in termites. Anim. Behav. 119, 179–187 (2016).

  19. 19.

    Rice, W. R., Friberg, U. & Gavrilets, S. Homosexuality as a consequence of epigenetically canalized sexual development. Q. Rev. Biol. 87, 343–368 (2012).

  20. 20.

    Rice, W. R., Friberg, U. & Gavrilets, S. Homosexuality via canalized sexual development: a testing protocol for a new epigenetic model. Bioessays 35, 764–770 (2013).

  21. 21.

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

  22. 22.

    Camin, J. H. & Sokal, R. R. A method for deducing branching sequences in phylogeny. Evolution 19, 311–326 (1965).

  23. 23.

    Prum, R. O. The Lande–Kirkpatrick mechanism is the null model of evolution by intersexual selection: implications for meaning, honesty, and design in intersexual signals. Evolution 64, 3085–3100 (2010).

  24. 24.

    Eberhard, W. Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, 1996).

  25. 25.

    Milam, E. L. Looking for a Few Good Males: Female Choice in Evolutionary Biology (JHU Press, 2010).

  26. 26.

    Kamath, A. & Losos, J. The erratic and contingent progression of research on territoriality: a case study. Behav. Ecol. Sociobiol. 71, 89 (2017).

  27. 27.

    Kamath, A. & Losos, J. Reconsidering territoriality is necessary for understanding Anolis mating systems. Behav. Ecol. Sociobiol. 72, 106 (2018).

  28. 28.

    Uller, T. & Olsson, M. Multiple paternity in reptiles: patterns and processes. Mol. Ecol. 17, 2566–2580 (2008).

  29. 29.

    Kokko, H. & Mappes, J. Multiple mating by females is a natural outcome of a null model of mate encounters. Entomol. Exp. Appl. 146, 26–37 (2013).

  30. 30.

    Tang-Martínez, Z. Rethinking Bateman’s principles: challenging persistent myths of sexually reluctant females and promiscuous males. J. Sex. Res. 53, 532–559 (2016).

  31. 31.

    Boulton, R. A., Zuk, M. & Shuker, D. M. An inconvenient truth: the unconsidered benefits of convenience polyandry. Trends Ecol. Evol. 33, 904–915 (2018).

  32. 32.

    Kekäläinen, J. & Evans, J. P. Gamete-mediated mate choice: towards a more inclusive view of sexual selection. Proc. R. Soc. B 285, 20180836 (2018).

  33. 33.

    Yun, L. et al. Competition for mates and the improvement of nonsexual fitness. Proc. Natl. Acad. Sci. USA 115, 6762–6767 (2018).

  34. 34.

    Kamath, A. & Losos, J. B. Estimating encounter rates as the first step of sexual selection in the lizard Anolis sagrei. Proc. R. Soc. B 285, 20172244 (2018).

  35. 35.

    DuVal, E. H. & Kapoor, J. A. Causes and consequences of variation in female mate search investment in a lekking bird. Behav. Ecol. 26, 1537–1547 (2015).

  36. 36.

    Sandrin, L., Meunier, J., Raveh, S., Walser, J.-C. & Kölliker, M. Multiple paternity and mating group size in the European earwig, Forficula auricularia. Ecol. Entomol. 40, 159–166 (2015).

  37. 37.

    Parker, G. A. The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. Cold Spring Harb. Perspect. Biol. 6, a017509 (2014).

  38. 38.

    Young, C. M., Tyler, P. A., Cameron, J. L. & Rumrill, S. G. Seasonal breeding aggregations in low-density populations of the bathyal echinoid Stylocidaris lineata. Mar. Biol. 113, 603–612 (1992).

  39. 39.

    McCarthy, D. A. & Young, C. M. Gametogenesis and reproductive behavior in the echinoid Lytechinus variegatus. Mar. Ecol. Prog. Ser. 233, 157–168 (2002).

  40. 40.

    Keesing, J. K., Graham, F., Irvine, T. R. & Crossing, R. Synchronous aggregated pseudo-copulation of the sea star Archaster angulatus Müller & Troschel, 1842 (Echinodermata: Asteroidea) and its reproductive cycle in south-western Australia. Mar. Biol. 158, 1163–1173 (2011).

  41. 41.

    Thornhill, R. & Alcock, J. The Evolution of Insect Mating Systems (Harvard Univ. Press, 1983).

  42. 42.

    Han, C. S. & Brooks, R. C. Same-sex sexual behaviour as a by-product of reproductive strategy under male–male scramble competition. Anim. Behav. 108, 193–197 (2015).

  43. 43.

    Vasey, P. L. Homosexual behavior in primates: a review of evidence and theory. Int. J. Primatol. 16, 173–204 (1995).

  44. 44.

    Hoving, H.-J. T., Fernández-Álvarez, F. Á., Portner, E. J. & Gilly, W. F. Same-sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid). Mar. Biol. 166, 33 (2019).

  45. 45.

    MacFarlane, G. R., Blomberg, S. P. & Vasey, P. L. Homosexual behaviour in birds: frequency of expression is related to parental care disparity between the sexes. Anim. Behav. 80, 375–390 (2010).

  46. 46.

    Gröning, J. & Hochkirch, A. Reproductive interference between animal species. Q. Rev. Biol. 83, 257–282 (2008).

  47. 47.

    Kyogoku, D. & Sota, T. Exaggerated male genitalia intensify interspecific reproductive interference by damaging heterospecific female genitalia. J. Evol. Biol. 28, 1283–1289 (2015).

  48. 48.

    Takakura, K.-I., Nishida, T. & Iwao, K. Conflicting intersexual mate choices maintain interspecific sexual interactions. Popul. Ecol. 57, 261–271 (2015).

  49. 49.

    Drury, J. et al. A general explanation for the persistence of reproductive interference. Am. Nat. 194, 268–275 (2019).

  50. 50.

    Greenway, G., Hamel, J. & Miller, C. W. A tangled web: why do some individuals mate with the wrong species? Integr. Comp. Biol. 59, E88 (2019).

  51. 51.

    Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970).

  52. 52.

    Parker, G. A. in Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.) 1–60 (Academic Press, 1984).

  53. 53.

    Warner, R. R., Shapiro, D. Y., Marcanato, A. & Petersen, C. W. Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females. Proc. R. Soc. B 262, 135–139 (1995).

  54. 54.

    Pischedda, A. & Rice, W. R. Partitioning sexual selection into its mating success and fertilization success components. Proc. Natl. Acad. Sci. USA 109, 2049–2053 (2012).

  55. 55.

    Greenway, E. V., Dougherty, L. R. & Shuker, D. M. Mating failure. Curr. Biol. 25, R534–R536 (2015).

  56. 56.

    Meston, C. M. & Buss, D. M. Why humans have sex. Arch. Sex. Behav. 36, 477–507 (2007).

  57. 57.

    Pruitt, J. N., Burghardt, G. M. & Riechert, S. E. Non-conceptive sexual behavior in spiders: a form of play associated with body condition, personality type, and male intrasexual selection. Ethology 118, 33–40 (2012).

  58. 58.

    Hasegawa, M. & Arai, E. Sexually dimorphic swallows have higher extinction risk. Ecol. Evol. 8, 992–996 (2017).

  59. 59.

    Martins, M. J. F., Puckett, T. M., Lockwood, R., Swaddle, J. P. & Hunt, G. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556, 366–369 (2018).

  60. 60.

    Engel, K. C., Männer, L., Ayasse, M. & Steiger, S. Acceptance threshold theory can explain occurrence of homosexual behaviour. Biol. Lett. 11, 20140603 (2015).

  61. 61.

    Marco, A. & Lizana, M. The absence of species and sex recognition during mate search by male common toads, Bufo bufo. Ethol. Ecol. Evol. 14, 1–8 (2002).

  62. 62.

    Bailey, N. W. & French, N. Same-sex sexual behaviour and mistaken identity in male field crickets, Teleogryllus oceanicus. Anim. Behav. 84, 1031–1038 (2012).

  63. 63.

    Snyder, R. E. & Ellner, S. P. Pluck or luck: does trait variation or chance drive variation in lifetime reproductive success? Am. Nat. 191, E90–E107 (2018).

  64. 64.

    Levin, S. A. Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1, 431–436 (1998).

  65. 65.

    Holt, R. D. On the evolutionary ecology of species’ ranges. Evol. Ecol. Res. 5, 159–178 (2003).

  66. 66.

    Futuyma, D. J. Evolutionary constraint and ecological consequences. Evolution 64, 1865–1884 (2010).

  67. 67.

    Gould, S. J. & Vrba, E. S. Exaptation — a missing term in the science of form. Paleobiology 8, 4–15 (1982).

  68. 68.

    Larson, G., Stephens, P. A., Tehrani, J. J. & Layton, R. H. Exapting exaptation. Trends Ecol. Evol. 28, 497–498 (2013).

  69. 69.

    Lloyd, E. A. Adaptationism and the logic of research questions: how to think clearly about evolutionary causes. Biol. Theor. 10, 10–1007 (2015).

  70. 70.

    Gowaty, P. A. & Hubbell, S. P. Reproductive decisions under ecological constraints: It’s about time. Proc. Natl. Acad. Sci. USA 106, 10017–10024 (2009).

  71. 71.

    Ganna, A. et al. Large-scale GWAS reveals insights into the genetic architecture of same-sex sexual behavior. Science 365, eaat7693 (2019).

  72. 72.

    Jankowiak, Ł., Tryjanowski, P., Hetmański, T. & Skórka, P. Experimentally evoked same-sex sexual behaviour in pigeons: better to be in a female-female pair than alone. Sci. Rep. 8, 1654 (2018).

  73. 73.

    Maklakov, A. A. & Bonduriansky, R. Sex differences in survival costs of homosexual and heterosexual interactions: evidence from a fly and a beetle. Anim. Behav. 77, 1375–1379 (2009).

  74. 74.

    Emlen, S. T. & Oring, L. W. Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977).

  75. 75.

    MacFarlane, G. R., Blomberg, S. P., Kaplan, G. & Rogers, L. J. Same-sex sexual behavior in birds: expression is related to social mating system and state of development at hatching. Behav. Ecol. 18, 21–33 (2007).

  76. 76.

    McDonald, G. C., Gardner, A. & Pizzari, T. Sexual selection in complex communities: integrating interspecific reproductive interference in structured populations. Evolution 72, 1025–1036 (2019).

  77. 77.

    McDonald, G. C. & Pizzari, T. Structure of sexual networks determines the operation of sexual selection. Proc. Natl Acad. Sci. USA 115, E53–E61 (2018).

  78. 78.

    Zuk, M. Feminism and the study of animal behavior. BioScience 43, 774–778 (1993).

  79. 79.

    Somerville, S. Scientific racism and the emergence of the homosexual body. J. Hist. Sex. 5, 243–266 (1994).

  80. 80.

    Gowaty, P. Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers (Springer Science & Business Media, 1997).

  81. 81.

    McHugh, S. Queer (and) animal theories. GLQ 15, 153–169 (2009).

  82. 82.

    Subramaniam, B. Ghost Stories for Darwin: The Science of Variation and the Politics of Diversity (Univ. Illinois Press, 2014).

  83. 83.

    Nelson, L. H. Biology and Feminism: A Philosophical Introduction (Cambridge Univ. Press, 2017).

  84. 84.

    Fuselier, L., Eason, P. K., Jackson, J. K. & Spaulding, S. Images of objective knowledge construction in sexual selection chapters of evolution textbooks. Sci. Educ. 27, 1–21 (2018).

  85. 85.

    Ah-King, M. & Nylin, S. Sex in an evolutionary perspective: just another reaction norm. Evol. Biol. 37, 234–246 (2010).

  86. 86.

    Kokko, H. Give one species the task to come up with a theory that spans them all: what good can come out of that? Proc. R. Soc. B 284, 20171652 (2017).

  87. 87.

    Sugita, N. Homosexual fellatio: erect penis licking between male Bonin flying foxes Pteropus pselaphon. PLoS ONE 11, e0166024 (2016).

  88. 88.

    Ambrogio, O. V. & Pechenik, J. A. When is a male not a male? Sex recognition and choice in two sex-changing species. Behav. Ecol. Sociobiol. 62, 1779–1786 (2008).

  89. 89.

    Shine, R. et al. Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia 2001, 82–91 (2001).

  90. 90.

    Young, L. C., Zaun, B. J. & VanderWerf, E. A. Successful same-sex pairing in Laysan albatross. Biol. Lett. 4, 323–325 (2008).

  91. 91.

    Martin, C. M., Kruse, K. C. & Switzer, P. V. Social experience affects same-sex pairing behavior in male red flour beetles (Tribolium castaneum Herbst). J. Insect Behav. 28, 268–279 (2015).

  92. 92.

    Vasey, P. L. Same-sex sexual partner preference in hormonally and neurologically unmanipulated animals. Annu. Rev. Sex. Res. 13, 141–179 (2002).

  93. 93.

    Vasey, P. L. & Jiskoot, H. The biogeography and evolution of female homosexual behavior in Japanese macaques. Arch. Sex. Behav. 39, 1439–1441 (2010).

  94. 94.

    Zuk, M. Family values in black and white. Nature 439, 917 (2006).

  95. 95.

    Roberts, T. M. & Thorson, R. E. Chemical attraction between adults of Nippostrongylus brasiliensis: description of the phenomenon and effects of host immunity. J. Parasitol. 63, 357–363 (1977).

  96. 96.

    Nakashima, Y., Sakai, Y., Karino, K. & Kuwamura, T. Female-female spawning and sex change in a haremic coral-reef fish, Labroides dimidiatus. Zool. Sci. 17, 967–971 (2000).

  97. 97.

    Kazmi, Q. B. & Tirmizi, N. M. An unusual behaviour in box crabs (Decapoda, Brachyura, Calappidae). Crustaceana 53, 313–314 (1987).

  98. 98.

    PLoS Neglected Tropical Diseases Issue Image | Vol. 7(8) August 2013. PLoS Negl. Trop. Dis. 7, ev07.i08 (2013).

  99. 99.

    Gowaty, P. A. Sexual terms in sociobiology: emotionally evocative and, paradoxically, jargon. Anim. Behav. 30, 630–631 (1982).

  100. 100.

    Storms, M. D. Theories of sexual orientation. J. Pers. Soc. Psychol. 38, 783–792 (1980).

  101. 101.

    Hensley, C., Tewksbury, R. & Wright, J. Exploring the dynamics of masturbation and consensual same-sex activity within a male maximum security prison. J. Mens. Stud. 10, 59–71 (2001).

  102. 102.

    Fenton, K. A., Johnson, A. M., McManus, S. & Erens, B. Measuring sexual behaviour: methodological challenges in survey research. Sex. Transm. Infect. 77, 84–92 (2001).

  103. 103.

    Wolff, M., Wells, B., Ventura-DiPersia, C., Renson, A. & Grov, C. Measuring sexual orientation: a review and critique of U. S. data collection efforts and implications for health policy. J. Sex. Res. 54, 507–531 (2017).

Download references

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/).

Author information

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.

Correspondence to Julia D. Monk.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

A correction to this article is available online at https://doi.org/10.1038/s41559-019-1064-2.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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) doi:10.1038/s41559-019-1019-7

Download citation