Same-sex sexual behaviour and selection for indiscriminate mating


The widespread presence of same-sex sexual behaviour (SSB) has long been thought to pose an evolutionary conundrum, as participants in SSB suffer the cost of failing to reproduce after expending the time and energy to find a mate. The potential for SSB to occur as part of an optimal strategy has received less attention, although indiscriminate sexual behaviour may be the ancestral mode of sexual reproduction. Here, we build a simple model of sexual reproduction and create a theoretical framework for the evolution of indiscriminate sexual behaviour. We provide strong support for the hypothesis that SSB can be maintained by selection for indiscriminate sexual behaviour, by showing that indiscriminate mating is the optimal strategy under a wide range of conditions. Further, our model suggests that the conditions that most strongly favour indiscriminate mating were probably present at the origin of sexual behaviour. These findings have implications not only for the evolutionary origins of SSB, but also for the evolution of discriminate sexual behaviour across the animal kingdom.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Optimal discrimination strategies and resulting SSB.

Data availability

This manuscript does not use data.

Code availability

Code to replicate results can be found on Dryad at


  1. 1.

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

    PubMed  Google Scholar 

  2. 2.

    Caballero-Mendieta, N. & Cordero, C. Enigmatic liaisons in Lepidoptera: a review of same-sex courtship and copulation in butterflies and moths. J. Insect Sci. 12, 138 (2012).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

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

    Google Scholar 

  4. 4.

    Monk, J. D., Giglio, E., Kamath, A., Lambert, M. R. & McDonough, C. E. An alternative hypothesis for the evolution of same-sex sexual behaviour in animals. Nat. Ecol. Evol. 3, 1622–1631 (2019).

    PubMed  Google Scholar 

  5. 5.

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

    Google Scholar 

  6. 6.

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

    PubMed  Google Scholar 

  7. 7.

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

    PubMed  Google Scholar 

  8. 8.

    Furuichi, T., Connor, R. & Hashimoto, C. in Primates and Cetaceans (eds Yamagiwa, J. & Karczmarski, L.) 385–408 (Springer, 2013).

  9. 9.

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

    PubMed  PubMed Central  Google Scholar 

  10. 10.

    Lombardo, M. P., Bosman, R. M., Faro, C. A., Houtteman, S. G. & Kluisza, T. S. Homosexual copulations by male tree swallows. Wilson Bull. 106, 555–557 (1994).

    Google Scholar 

  11. 11.

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

    CAS  PubMed  Google Scholar 

  12. 12.

    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).

    Google Scholar 

  13. 13.

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

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    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).

    Google Scholar 

  15. 15.

    Harari, A. R., Brockmann, H. J. & Landolt, P. J. Intrasexual mounting in the beetle Diaprepes abbreviates (L.). Proc. R. Soc. B 267, 2071–2079 (2000).

    CAS  PubMed  Google Scholar 

  16. 16.

    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).

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Bailey, N. W., Hoskins, J. L., Green, J. & Ritchie, M. G. Measuring same-sex sexual behaviour: the influence of the male social environment. Anim. Behav. 86, 91–100 (2013).

    Google Scholar 

  18. 18.

    Martin, F. 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).

    Google Scholar 

  19. 19.

    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).

    PubMed  Google Scholar 

  20. 20.

    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).

    Google Scholar 

  21. 21.

    Hoving, H. J. T., Bush, S. L. & Robison, B. H. A shot in the dark: same-sex sexual behaviour in a deep-sea squid. Biol. Lett. 8, 287–290 (2011).

    PubMed  PubMed Central  Google Scholar 

  22. 22.

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

    Google Scholar 

  23. 23.

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

    Google Scholar 

  24. 24.

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

    Google Scholar 

  25. 25.

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

    Google Scholar 

  26. 26.

    Werner, Y. L. Apparent homosexual behavior in an all-female population of a lizard, Lepidodactylus lugubris and its probable interpretation. Z. Tierpsychol. 54, 144–150 (1980).

    Google Scholar 

  27. 27.

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

    Google Scholar 

  28. 28.

    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, 967–970 (2000).

    Google Scholar 

  29. 29.

    Shine, R. et al. Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia 1, 82–91 (2001).

    Google Scholar 

  30. 30.

    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).

    Google Scholar 

  31. 31.

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

    PubMed  Google Scholar 

  32. 32.

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

    PubMed  Google Scholar 

  33. 33.

    Dickins, T. E. & Rahman, Q. Ancestral primacy of same-sex sexual behaviour does not explain its stable prevalence in modern populations. Nat. Ecol. Evol. 4, 782–783 (2020).

    CAS  PubMed  Google Scholar 

  34. 34.

    Spratt, E. C. Male homosexual behaviour and other factors influencing adult longevity in Tribolium castaneum (Herbst) and T. confusum Duval. J. Stored Prod. Res. 16, 109–114 (1980).

    Google Scholar 

  35. 35.

    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, 1375–1397 (2009).

    Google Scholar 

  36. 36.

    Stojkovic, B., Jovanovic, D. S., Tucic, B. & Tucic, N. Homosexual behaviour and its longevity cost in females and males of the seed beetle Acanthoscelides obtectus. Physiol. Entomol. 35, 308–316 (2010).

    Google Scholar 

  37. 37.

    Doebeli, M., Ispolatov, Y. & Simon, B. Towards a mechanistic foundation of evolutionary theory. eLife 6, e23804 (2017).

    PubMed  PubMed Central  Google Scholar 

  38. 38.

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

    Google Scholar 

  39. 39.

    Macchiano, A., Razik, I. & Sagot, M. Same-sex courtship behaviors in male-biased populations: evidence for the mistaken identity hypothesis. Acta Ethol. 21, 147–151 (2018).

    Google Scholar 

  40. 40.

    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).

    Google Scholar 

  41. 41.

    Steiger, S. & Muller, J. K. From class-specific to individual discrimination: acceptance threshold changes with risk in the partner recognition system of the burying beetle Nicophorus vespilloides. Anim. Behav. 80, 607–613 (2010).

    Google Scholar 

  42. 42.

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

    Google Scholar 

  43. 43.

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

    PubMed  PubMed Central  Google Scholar 

  44. 44.

    Reeve, H. K. The evolution of conspecific acceptance thresholds. Am. Nat. 133, 407–435 (1989).

    Google Scholar 

  45. 45.

    Roughgarden, J. in Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People (ed. Roughgarden, J.) Ch. 8 (Univ. California Press, 2004).

  46. 46.

    Mann, J. Homosexual Behaviour in Animals: An Evolutionary Perspective (eds Sommer, V. & Vasey, P. L.) Ch. 4 (Cambridge Univ. Press, 2006).

  47. 47.

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

    Google Scholar 

  48. 48.

    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).

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Godin, J. J. & Briggs, S. E. Female mate choice under predation risk in the guppy. Anim. Behav. 51, 117–130 (1996).

    Google Scholar 

  50. 50.

    Byers, J. A., Byers, A. A. & Dunn, S. J. A dry summer diminishes mate search effort by pronghorn females: evidence for a significant cost of mate search. Ethology 112, 74–80 (2006).

    Google Scholar 

  51. 51.

    Bluhm, B. A., Piepenburg, D. & von Jeterzenka, K. Distribution, standing stock, growth, mortality, and production of Stronglyocentrotus pallidus (Echinodermata: Echinoidea) in the northern Barents Sea. Polar Biol. 20, 325–334 (1998).

    Google Scholar 

  52. 52.

    Ebert, T. A., Russell, M. P., Gamba, G. & Badnar, A. Growth, survival, and longevity estimates for the rock-boring sea urchin Echinometra lucunter lucenter (Echinodermata, Echinoidea) in Bermuda. Bull. Mar. Sci. 82, 381–403 (2008).

    Google Scholar 

  53. 53.

    Miller, R. L. Evidence for the presence of sexual pheromones in free-spawning starfish. J. Exp. Mar. Biol. Ecol. 130, 205–221 (1989).

    CAS  Google Scholar 

  54. 54.

    Mercier, A. & Hamel, J.-F. in Endogenous and Exogenous Control of Gametogenesis and Spawning in Echinoderms (eds Mercier, A. & Hamel, J.-F.) Ch. 3 (Academic, 2009).

  55. 55.

    Slattery, M. & Bosch, I. Mating behavior of a brooding Antarctic asteroid Neosmilaster georgianus. Invertebr. Reprod. Dev. 24, 97–102 (1993).

    Google Scholar 

  56. 56.

    Bulmer, M. Structural instability of models of sexual selection. Theor. Pop. Biol. 35, 195–208 (1989).

    CAS  Google Scholar 

Download references


We thank M. Moore and M. Lambert for comments on early versions of the manuscript and A. Deconinck for suggesting the name ‘targeted’ sex. M.R.S. was supported by the National Science Foundation with award no. DEB-1939290.

Author information




B.A.L. conceived of the project and the optimization models. B.A.L. and M.R.S. designed the population genetic models. B.A.L. led the writing on the manuscript with input from M.R.S.

Corresponding author

Correspondence to Brian A. Lerch.

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.

Supplementary information

Supplementary Information

Supplementary Fig. 1, Methods and Appendices 1–4.

Reporting Summary

Supplementary Video 1

Video showing the fitness gradient as a function of attempted discrimination a changing with each parameter. The default setting for each parameter is c = 0.1, s = 1, σ = 0.5, d = 0.8, f = 1, p = 0 and r = 0. Each parameter is allowed to vary between 0 and 1, except for c, which is allowed to vary only between 0 and 0.2, and d, which is allowed to vary between 0 and 0.9. Evolutionary optima occur wherever the line crosses the x axis (and has a negative slope). If the line is always positive, the optimal strategy is to always discriminate. If the line is always negative, the optimal strategy is to never attempt sexual discrimination.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lerch, B.A., Servedio, M.R. Same-sex sexual behaviour and selection for indiscriminate mating. Nat Ecol Evol 5, 135–141 (2021).

Download citation


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing