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.
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This manuscript does not use data.
Code to replicate results can be found on Dryad at https://doi.org/10.5061/dryad.gxd2547jg.
Bailey, N. W. & Zuk, M. Same-sex sexual behavior and evolution. Trends Ecol. Evol. 24, 439–446 (2009).
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).
Scharf, I. & Martin, O. Y. Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences. Behav. Ecol. Sociobiol. 67, 1719–1730 (2013).
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).
Vasey, P. L. Homosexual behavior in primates: a review of evidence and theory. Int. J. Primatol. 16, 173–204 (1995).
Vasey, P. L. Same-sex sexual partner preference in hormonally and neurologically unmanipulated animals. Annu. Rev. Sex Res. 13, 141–179 (2002).
Vasey, P. L. & Jiskoot, H. The biogeography and evolution of female homosexual behavior in Japanese macaques. Arch. Sex. Behav. 39, 1439–1441 (2010).
Furuichi, T., Connor, R. & Hashimoto, C. in Primates and Cetaceans (eds Yamagiwa, J. & Karczmarski, L.) 385–408 (Springer, 2013).
Sugita, N. Homosexual fellatio: erect penis licking between male Bonin flying foxes Pteropus pselaphon. PLoS ONE 11, e0166024 (2016).
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).
Zuk, M. Family values in black and white. Nature 439, 917 (2006).
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).
Young, L. C., Zaun, B. J. & VanderWerf, E. A. Successful same-sex pairing in Laysan albatross. Biol. Lett. 4, 323–325 (2008).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
McCarthy, D. A. & Young, C. M. Gametogenesis and reproductive behavior in the echinoid Lytechinus variegatus. Mar. Ecol. Prog. Ser. 233, 157–168 (2002).
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).
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).
Kazmi, Q. B. & Tirmizi, N. M. An unusual behavior in box crabs (Decapoda, Brachyura, Calappidae). Crustaceana 53, 313–314 (1987).
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).
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).
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).
Gavrilets, S. & Rice, W. R. Genetic models of homosexuality: generating testable predictions. Proc. R. Soc. B 273, 3031–3038 (2006).
Rice, W. R., Friberg, U. & Gavrilets, S. Homosexuality as a consequence of epigenetically canalized sexual development. Q. Rev. Biol. 87, 343–368 (2012).
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).
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).
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).
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).
Doebeli, M., Ispolatov, Y. & Simon, B. Towards a mechanistic foundation of evolutionary theory. eLife 6, e23804 (2017).
Bailey, N. W. & French, N. Same-sex sexual behaviour and mistaken identity in male field crickets, Teleogryllus oceanicus. Anim. Behav. 84, 1031–1038 (2012).
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).
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).
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).
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).
Engel, K. C., Manner, L., Ayasse, M. & Steiger, S. Acceptance threshold theory can explain occurrence of homosexual behaviour. Biol. Lett. 11, 20140603 (2015).
Reeve, H. K. The evolution of conspecific acceptance thresholds. Am. Nat. 133, 407–435 (1989).
Roughgarden, J. in Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People (ed. Roughgarden, J.) Ch. 8 (Univ. California Press, 2004).
Mann, J. Homosexual Behaviour in Animals: An Evolutionary Perspective (eds Sommer, V. & Vasey, P. L.) Ch. 4 (Cambridge Univ. Press, 2006).
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).
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).
Godin, J. J. & Briggs, S. E. Female mate choice under predation risk in the guppy. Anim. Behav. 51, 117–130 (1996).
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).
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).
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).
Miller, R. L. Evidence for the presence of sexual pheromones in free-spawning starfish. J. Exp. Mar. Biol. Ecol. 130, 205–221 (1989).
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).
Slattery, M. & Bosch, I. Mating behavior of a brooding Antarctic asteroid Neosmilaster georgianus. Invertebr. Reprod. Dev. 24, 97–102 (1993).
Bulmer, M. Structural instability of models of sexual selection. Theor. Pop. Biol. 35, 195–208 (1989).
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.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Fig. 1, Methods and Appendices 1–4.
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.
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Lerch, B.A., Servedio, M.R. Same-sex sexual behaviour and selection for indiscriminate mating. Nat Ecol Evol 5, 135–141 (2021). https://doi.org/10.1038/s41559-020-01331-w