Let’s start with the basics of sexual reproduction, which might appear simple enough, but across the animal kingdom are in fact incredibly diverse and messy. Some of the descriptions of sex that follow will sound familiar to us, other acts less so, I hope. But to get to grips with the complexities of our own sexual behaviour, we must indulge in a brief survey of the sex lives of other animals.
There are many ways to be sexual, though they broadly fit into two categories. The first of these is species that have two sexes, which we traditionally call male and female. In mammals, sex is determined by discrete packages of DNA called chromosomes. We inherit a set of twenty-three chromosomes from each parent, which are matched as pairs, except for the fact that one of the pairs is not a matching pair half of the time: females have two X chromosomes, but males have an X and a Y. The female egg contains one set of chromosomes, including an X, and every sperm contains another set, each one either bearing an X or a Y. In reptiles, birds and butterflies, it’s the other way around (with slightly different but irrelevant annotation: males are WW, and females are WZ).
But that’s not the only way to determine sex. In some animals, maleness and femaleness is not governed by the presence of certain chromosomes, but by where you are conceived: for lots of reptiles, sex is temperature dependent, meaning that differences of as little as one degree Celsius in where an egg is placed in relation to others will determine whether that egg is a male or female. For some reptile species, an egg in the centre of a clutch will be slightly warmer, and will therefore develop as male. For the strange New Zealand reptile the tuatara, it’s the other way around. In crocodiles, you become a female if you’re a particularly hot or cold egg, and male if you’re somewhere in the middle. And so it goes. Ours is but one of myriad ways that males and females can be made.
In the second broad category of being a sexual organism are the species that have dozens of sexes, possibly thousands. Mostly these are mushrooms and other types of fungi, which we don’t normally think of as sexual but are nonetheless. They have what are called ‘mating types’, which are sections of DNA that are variable between individuals, and simply indicate to a potential mate that they are different enough to warrant sex. Mates are hard to find if you are a mushroom, as they’re pretty slow-moving, and sex doesn’t happen very often, so a rare chance encounter with another lonely mushroom who happens to be the same sex type as yourself is a disaster. It therefore pays to have as many options as possible, and the best way is for you to have many mating types as long as none of them is yours.
Mushrooms aside, most sexual organisms fall into the male-and-female category. Compared to the many permutations of fungi, when it comes to sexual reproduction that includes males and females, the act itself is mesmerisingly diverse. Penis in vagina is but one way. That’s an old technique, as in the case of the prehistoric Dunkleosteus, mentioned above. Many insects, such as the bedbug Cimex lectularius, aren’t that fussed about a specific entrance for penetration, and a male will pierce the abdomen of his mate with a very pointy scythe-like aedeagus (equivalent to a penis), and the sperm will find their way to the eggs via the internal organs of the female. We call this ‘traumatic insemination’.
Plenty of animals don’t engage in penetrative sex at all, and external fertilisation is how it’s done. As with many fish, male and female Chinook salmon release their sperm and eggs into the water, and the ovarian fluid that envelops the eggs acts as a highly selective filter; some sperm are simply able to swim faster through this gel than others, and this skill appears to be determined genetically by the females: their fluids act as a filter for the best and most genetically suited swimmers. Birds tend not to have penises, and so transfer sperm via a ‘genital kiss’, where egg and sperm meet near the cloacal entrance/exit, and are internalised by the female. That’s the case for most birds, but not all. The Argentine ruddy duck has a corkscrew penis, which twists in the opposite direction to the female’s tortuous corkscrew vagina, thus allowing her to retain a degree of control over who sires her ducklings.
With competition for reproductive rights being so fierce, some aspects of sex are not designed solely to impregnate the female, but to simply prevent another male from becoming the father. As in all sporting competitions, there are defensive strategies and offensive strategies. In defence: many creatures across the whole domain of animals use copulatory plugs, physical barriers inserted after sex to prevent another male from delivering their sperm successfully. In offence: some male flies release toxic semen to poison any further attempts. Some fish and some flies store their sperm in compartments, and can regulate how much they release, which is dependent on how many males have had sex with a female already, and where they are in the rank. The simplest tactic is to merely hang around long after you are welcome, and in some cases while still locked in coitus. Dogs do this, and sometimes you might see a pair of them in flagrante for half an hour or so in a local park, the female dragging the male round on her back. Dog penises have a section of erectile tissue called the knot (or more properly, bulbus glandis) which helps the dog sustain an enlarged erection after ejaculation, causing a vaginal anchor for a time, which has the simple effect of preventing another male from assuming the same position. Not particularly sophisticated, but quite effective.
While there are many ways that males and females can do it, plenty of animals aren’t so binary. Sexual reproduction that features two sexes doesn’t necessarily mean that there are two different types of organism or gender. Many creatures are hermaphrodites, and bear both sexual types in one body. Flowering plants are like this of course, carrying both pollen and ovules, the botanical equivalent of sperm and egg. The earliest recorded example of sexual reproduction comes from an alga, with the perfect name Bangiomorpha pubescens, fossilised around a billion years ago in what is now Canadian shale. In microscopic slices through these fossils we can see sexual spores, equivalent to sperm and egg.
Female Komodo dragons are capable of parthenogenesis when the situation requires it. This means that they can conceive without ever having had any contact with a male – literally a virgin birth – and in the absence of a sex chromosome from a father, all her offspring will be male. Komodo lifestyles are fairly solitary, and they may not come across potential mates very often. This way, she can mate with her sons without needing to have encountered a male (though this is a last resort, as it is not a great idea over multiple generations; with no new genetic information that would be provided by a father, they soon become profoundly and dangerously inbred).
Then there is the drama enacted by organisms such as the flatworms. When a couple of hermaphrodite Pseudobiceros hancockanus feel the urge to reproduce, two of them coil around each other and engage in an aggressive head-to-head wrestle with weapons drawn, an act which has the scientific designation of ‘penis fencing’. Whichever worm wins does so by piercing the head of the other with its spiked organ, and coerces the loser into adopting the female role in this relationship, and becoming the sperm receptacle and egg bearer. It’s easier to produce sperm than it is eggs, and it’s harder to bear the younglings, so the individual who managed to claim the male mantle remains childfree, and ready to crack on for another round with a new individual. And they say romance is dead.
On the great evolutionary tree of life, flatworms are animals almost as far away from us as any, but penis fencing occurs in much more closely related beasts, including the mammals. Plenty of whales lock horns in this manner, and our even closer mammalian cousins the bonobos touch swords to resolve conflict, to make friends, and even when getting excited about a forthcoming meal (though this jousting is merely competitive rather than resulting in full penetration).
Wrasse, groupers and clownfish are sequential hermaphrodites. These fish tend to have strict social hierarchies, with a dominant female who mothers the whole brood. If the dominant female clownfish is removed, perhaps by being eaten, then as a result of an absence of her hormones among the group, a male – typically the largest – will move up a rung on the heavily stratified social ladder, and will spontaneously undergo a radical sex change. His testes will atrophy and he’ll grow ovaries, and over the course of a couple of days, he becomes she. The fish will balloon, becoming a replacement dominant female.1
Social structure in nature plays a big part in how the sexes are organised. Bees, wasps and ants have two sexes, but equality is far from their hive-minds. Males only have half a genome, and their lives are defined by just two jobs: protecting the queen and the colony, and having sex with the females on demand. They are literally sex slaves. If these insects seem far from our own clade, two species of mammal also use a similar system. The social structure of naked mole rats and Damaraland mole rats includes a fertile queen and a couple of mating males, while the rest are sterile male workers – some tunnellers, others soldiers.
Being a sex slave might be a better deal than the male Australian redback spider gets, whose best evolutionary tactic is to provide the ultimate dinner date – immediately after releasing his sperm to a receptive female he is eaten by her. If she is eating, she is preoccupied, and sated with nutritious food that will help nurture her spiderlings, and therefore she is less likely to mate with another male spider, who might displace the first one’s sperm. This strategy is known as ‘reproductive cannibalism’ – possibly the least sexy phrase ever devised.
Another model of courtship in animals has a much better scientific name. In socially stratified organisms, it pays for females to occasionally mate with a male who is not an alpha, but this is not always easy – and is potentially lethal – for a sub-alpha male. Plenty of tactics exist to distract the dominant males long enough to sneak a quick sexual encounter. Barn swallows will raise the alarm call of an aerial threat from above, in order to quickly and cautiously mate, while the duped birds are evading a fictional attack. Most demonstrative of all are the cuttlefish Sepia plangon. Males looking for opportunistic and safe sex with a female will change their colour patterns on the side facing the dominant males so that it resembles a female. The dominant males assume no mating competition, and the temporarily effete male gets potential access to a female that would otherwise result in the furious ire of a dominant male. This heinous perfidy is officially known as ‘kleptogamy’ – stolen mating – but no one calls it that. The great evolutionary biologist John Maynard Smith gave it a much better name, which is used universally in evolutionary circles: the ‘sneaky fucker strategy’.
You might wince – or nod appreciatively – at these acts being so apparently similar or different from the way we do it. It might seem tempting to assume that a recognition of some of these behaviours in us indicates a common ancestral route. Here we must be careful. Reproduction based on organisms having male and female parts is clearly an ancient business, but the details of how this plays out in specific organisms may be independent of each other. The sex acts we see in nature do not necessarily have homologues in us, no matter how similar they may seem.
Of course, the most numerous and successful domains of life – the bacteria and archaea – do not have sex at all, and merely undergo binary fission, splitting in two to pass their genes into the future.2 But among the beasts (and plants and fungi), sex is clearly a smart trick to have in your evolutionary backpack, and has evolved in a multitude of ways that appear sometimes familiar and sometimes totally alien to us.
1 Removal of the dominant female clownfish is the opening to the excellent 2003 film Finding Nemo. The plucky titular protagonist is the smallest and only remaining offspring in the shoal and is then raised by his father, before an exciting adventure unfolds. The biologically accurate version of this film would have the father, Marlin, physically transforming into a female, and then having sex with his own son, but I guess that would be a different, possibly less popular, story.
2 They do a sort of version of sex, where genes can be passed from individual cell to individual cell. One extends a pilus (Latin for ‘spear’) and passes a small loop of DNA from one to another. This process, called ‘horizontal gene transfer’, is why we humans currently face a great crisis with antibiotic resistance. Once a useful trait (such as resistance to an otherwise lethal drug) evolves in one cell, it can be passed around quickly and at will. This is also the reason why the root of the tree of life, before complex life arose some 2.4 billion years ago, is nothing like a tree at all, but instead a matted web, with no distinct branches, just a net of gene flow from every one of the billions of cells under the sun.