Same-sex sexual behaviour can be maintained by selection for indiscriminate sexual behaviour because indiscriminate mating is the optimal strategy under a wide range of conditions

Same-sex sexual behaviour and selection for indiscriminate mating. Brian A. Lerch & Maria R. Servedio. Nature Ecology & Evolution, Nov 9 2020. https://www.nature.com/articles/s41559-020-01331-w

Abstract: 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.

Empirical observations of SSB (that is, any attempted sexual activity between two or more members of the same sex) in ani-mals are widespread1–4, with evidence of SSB in mammals5–9, birds10–14, arthropods15–19, molluscs20–22, echinoderms23–25 and other animals26–30. Since SSB is traditionally thought to be deleterious, as same-sex matings require energy expenditure but cannot produce offspring, there has been much interest in understanding its origin and maintenance1–5. Despite this, there exists no strong theoretical foundation for understanding SSB (but see refs. 31,32), resulting in a wide range of untested verbal arguments in the literature1–5.Recently, Monk et al.4 challenged the long-standing perspective of SSB as a derived trait, arguing that rather than trying to under-stand its presence, a more salient question would be to understand its absence. They hypothesize that indiscriminate sexual behav-iour (that is, mating without determining the sex of one’s part-ner) is the ancestral condition, realizing that discriminate sexual behaviour (that is, directing sexual behaviour at members of the opposite sex) must evolve through mechanisms controlling sexual signalling and mate choosiness. Of course, the existence of indis-criminate mating as the ancestral condition does not explain its current prevalence33. While in some cases (for example, broadcast spawning and wind pollination) indiscriminate mating predomi-nates as a result of little potential benefit to (or opportunity for) sexual discrimination, it is oftentimes unclear why indiscriminate mating persists.Building on the perspective of Monk et al.4, we argue that selec-tion may actually favour indiscriminate sexual behaviour (or pre-vent the evolution of sexual discrimination) under a wide range of conditions observed in nature. We create a theoretical framework for understanding the conditions that favour indiscriminate sexual behaviour and provide a test of whether SSB is likely to result from selection for indiscriminate sexual behaviour. We start with a sim-ple optimization model of sexual reproduction, and then support this approach with a population genetic model that explicitly tracks evolutionary dynamics. We find that indiscriminate mating is the optimal strategy for many parameter combinations and produce testable predictions about the conditions that favour SSB resulting from indiscriminate mating.