For a very long time, scientists have known that animals engage in sexual behavior with individuals of the same sex. Such same-sex sexual behavior (SSB)* can include, for example, mounting, courting through songs and other signals, genital licking or releasing sperm, and has been observed in over 1,500 animal species, from primates to sea stars, bats to damselflies, snakes to nematode worms.

In recent decades, numerous hypotheses have been proposed and tested to understand why animals engage in these sexual behaviors that do not directly lead to reproduction. In a theoretical perspective published in Nature Ecology and Evolution, we reflect on the hypotheses proposed by biologists to explain SSB, and on the widespread but unquestioned assumptions that underlie them.

Common to all the hypotheses proposed to explain SSB is the characterization of SSB as an “evolutionary paradox” because it persists without obviously contributing to an animal’s survival or reproductive success (what biologists call “fitness”). As a “paradox,” SSB is assumed by biologists to be so obviously costly that it must either yield tremendous benefits or be otherwise impervious to elimination by natural selection.

Moreover, most scientists who study SSB tend to focus exclusively on its presence in a single species of interest, leading to the unacknowledged assumption that SSB evolved independently in each of the animal species in which it is observed. But are these assumptions well-founded? We argue that they are not, and that they are perhaps rooted more in cultural norms than in scientific rigor.

First, the costs of SSB are often assumed to be high because engaging in SSB leads individuals to waste time, energy and resources without obvious gains in fitness. The costliness of SSB is often emphasized in comparison to the benefits of having sex with an individual of a different sex (different-sex sexual behavior or DSB). While DSB can certainly lead more obviously to higher fitness through the production of offspring, these comparisons assume that DSB is highly efficient.

However, animals often mate many times to produce just a few offspring, and acts of DSB frequently do not result in reproduction for a whole host of reasons. In other words, DSB can be costly too, and it is rarely clear whether mating with an individual of the same sex is comparatively costlier than any other reason why sexual behavior may not lead to reproduction.

Second, for other traits that are as widespread across so many species as SSB, biologists often consider the evolutionary possibility that the trait evolved just once or a few times in the species’ common ancestor, rather than many independent times. As far as we can tell, no such evolutionary scenario has been considered for SSB. Finally, both of these assumptions underlying previous research on SSB are reinforced by a heteronormative worldview under which SSB is seen as aberrant, perhaps explaining where these assumptions came from and why they were so rarely questioned.

In our paper, we argue for a subtle shift in perspective that offers new ways of understanding the diverse and endlessly fascinating world of animal sex, including SSB. We explicitly move away from viewing SSB as aberrant or as mutually exclusive from DSB, instead acknowledging that individuals and populations of animals can engage in a spectrum of sexual behaviors that include both DSB and SSB in a vast array of combinations.

This perspective leads us to propose the following alternative scenario: what if SSB has been around since animals began to engage in sexual behavior of any kind? In our hypothesis, the ancestral animal species mated indiscriminately with regard to sex, i.e., they mated with individuals of all sexes, if only because it is unlikely that the other traits required to recognize a compatible mate—differences in size, shape, color or odor, for example—evolved at exactly the same time as sexual behaviors.

Indeed, indiscriminate mating can be more beneficial than it is costly. Mate recognition can require physiologically and cognitively costly adaptations, and being excessively discriminating in choosing mates can lead individuals to miss out on mating opportunities that lead to reproduction, a significant fitness cost.

And so, we hypothesize that present-day diversity in sexual behavior in animals stems from an ancestral background of indiscriminate mating among individuals of all sexes. In some branches of the animal tree of life, where SSB is actually quite costly, this behavior might be selected against.

But in other taxa where SSB isn’t relatively costly, it may have persisted and even been co-opted to serve other beneficial functions. Scientists currently lack comprehensive knowledge of how common SSB is across species, largely because these behaviors have historically been regarded as unseemly or irrelevant and have only been recorded incidentally. We predict that the systematic documentation of SSB across animal taxa, and the quantification of the costs and benefits of both SSB and DSB, would reveal that it is both more common and less costly than is currently widely assumed.

In presenting our hypothesis of the ancestral origins for SSB in animals, we suggest nothing about conceptualizing human sexual behavior. It should never be the place of science to make normative arguments about people. Indeed, we suggest that human culture has likely had far more impact on the study of biology than vice versa. Instead, we hope our hypothesis will expand understanding of the diversity of the natural world. We encourage scientists to consider what discoveries in evolutionary biology are possible when we break free from the cultural norms and assumptions that have historically constrained scientific creativity.

In this regard, scientists have much to learn from other disciplines, such as science and technology studies (STS), that apply critical lenses to the processes of science. Interdisciplinary collaboration with scholars in such fields has the potential to make science more robust by teaching scientists to account for the inevitable role society and culture play in all forms of research.

The questions we ask shape our understanding of the world, but these questions are also shaped by our understanding of the world. Who we are influences the hypotheses we craft and the assumptions we make. Thus, scientists should be thoughtful about the critical lenses, biases and assumptions we bring to the process of asking questions, designing experiments and interpreting results. Widening the range of perspectives and cultures that have a voice in academic science is critical to the improvement of scientific practice and knowledge-building. Who knows what hypotheses new voices will bring to science in the future?

*Note: We intentionally do not use terms such as “heterosexual” or “homosexual” to prevent any conflation between human sexuality and nonhuman animal sexual behaviors. Moreover, the terms same-sex sexual behavior (SSB) and different-sex sexual behavior (DSB) more accurately describe the observation of individual sexual interactions, without making assumptions as to how those same individuals may behave in other encounters.