The Diversity of Sexuality: A Window into Evolutionary History

I was recently reminded in conversation of a topic in biology that I find fascinating, not only due to the sometimes described ‘paradoxical’ evolutionary nature of its existence, but also due to the potential biases that have surrounded its study for centuries.
 
Across the vast diversity of the animal kingdom, one behaviour has often baffled biologists: same-sex sexual behaviour. This is not the same as a homosexual orientation in humans, which more closely aligns with what is referred to as same-sex sexual preference (i.e. when individuals are more likely to undergo sexual behaviour with individuals of the same sex as themselves when different-sex partners are available). From penguins to primates, and even insects, same-sex sexual behaviour is common across species (for a great book on this, see Joan Roughgarden’s “Evolution’s Rainbow”, or Bailey and Zuk’s shorter review paper). But why would animals invest in behaviours that don't directly lead to reproduction? Isn’t that an evolutionary dead-end? This question has sparked many studies, arguments and controversy among the research community, with scientists traditionally framing same-sex sexual behaviour as an evolutionary costly behaviour that begs for an adaptive explanation. An alternative perspective, however, turns this idea on its head: the "ancestral indiscriminate sexual behaviour" hypothesis.
 
This challenges the notion that animals evolved from ancestors engaging exclusively in different-sex sexual behaviour, from which same-sex sexual behaviour has evolved. Instead, it suggests that the earliest sexual behaviours weren’t sex-specific at all, but animals directed their mating efforts at whoever was available, regardless of sex. Could this ancestral state explain the persistence of same-sex sexual behaviour in the animal kingdom today?
 
To understand this, we must imagine the world’s first sexually-reproducing animals. These were different to the complex multicellular animals that we are used to seeing on our TV screens today, with nature documentaries often showcasing male animals jostling it out to impress the females and attain mating opportunities. Long before elaborate courtship rituals emerged, these ancestral species didn’t have the ability to finely-tune mate recognition. Instead, we must picture a much simpler organism, consisting of just one cell. Billions of years ago, these single cells began to swap, shuffle and merge their DNA with one another, creating new cells with unique genetic combinations. While it may not resemble the intricate processes we see today, this was the humble beginning of sexual reproduction and behaviour.
 
Sexual reproduction gave organisms an edge over asexual ones by mixing genetic material, allowing offspring to adapt better to changing environments compared to clones produced through asexual reproduction. As is often the case in evolution, this new method of reproduction sparked competition between individuals, where some cells wanted to become smaller and more mobile to increase their chances of fertilising others. Because these smaller cells contributed fewer resources to new offspring, it became necessary for other cells to evolve to become larger and more nutrient-rich, so that new and developing offspring had enough energy to survive. It was this evolutionary race for reproduction that ultimately led to the evolution of biological sex, where two distinct sex cells (called gametes) evolved: male sperm and female eggs.
 
The crux of the ancestral indiscriminate sexual behaviour hypothesis lies in this evolutionary timeline of events that led to sexual reproduction and biological sex. For sperm and eggs to evolve, sexual reproduction must have come first. As a result, the earliest sexual behaviours were likely ‘indiscriminate’, aimed at increasing mating opportunities by attempting to reproduce with all individuals rather than selecting partners based on their biological sex, which was in the early stages of evolving. The result? A natural mix of same-sex and different-sex interactions.
 
For those early species, life was all about maximising reproductive success in challenging environments. Picture a group of primitive animals releasing eggs and sperm into the ocean. The goal was simple: fertilise as many cells as possible. In such scenarios, being overly selective about your mate’s sex could backfire. By directing sexual behaviour indiscriminately, individuals increased their odds of successful reproduction. In this ancestral world, missed opportunities could be far more costly than the occasional same-sex interaction. Evolution, after all, isn’t all about perfection, it’s about what works well enough to pass on genes.
 
The hypothesis therefore suggests that same-sex sexual behaviour isn’t some evolutionary oddity that evolved later, but instead it was simply part of the package. In fact, targeting sexual behaviour exclusively toward the opposite sex may be the derived, more specialised trait that evolved in specific contexts. In other words, same-sex sexual behaviour hasn’t evolved repeatedly in specific animal groups as many scientists have previously argued, but instead persists as a relic of the earliest sexual behaviours.
 
This perspective allows us to recognise some of the biases that have historically stung scientific research. Much of the 19th- and 20th-century work on same-sex sexual behaviour was likely prejudiced by heteronormative assumptions and Euro-American cultural norms, where discrimination against queer individuals may have contributed to framing same-sex behaviour as unnatural or in need of special justification. By shifting our baseline to consider indiscriminate sexual behaviour as the ancestral state, we can move beyond these biases and gain a clearer understanding of the rich diversity in animal behaviour. It reminds us that same-sex sexual behaviour is part of a broader, ancient behavioural repertoire, not some unusual exception.
 
It's important to approach this shift with caution, as science can sometimes be coopted to support subjective and dated beliefs about what is ‘natural’ in humans. It seems in modern times we are frequently seeing science being misused to justify discriminatory positions on gender, sexuality, and behaviour, such as rigid gender ideologies or assumptions about what human identities should or shouldn’t be. This risks oversimplifying complex biological and social phenomena and inappropriately applying conclusions from the animal kingdom to human society.
 
However, the ancestral indiscriminate sexual behaviour hypothesis provides a fresh lens through which to view same-sex sexual behaviour. It suggests that this behaviour isn’t an evolutionary paradox or a costly mistake, it’s a window into the ancient roots of animal behaviour. By recognising same-sex sexual behaviour as a natural and persistent trait, we can better appreciate the diversity of life and evolution’s complex, intricate and messy beauty.