The Twisted World of Sexual Organs

How evolution solved the problem of conception

It's February 2008. The location; a hospital emergency department within the city of Seoul, in South Korea.

A 63-year-old woman has arrived complaining of sharp pains in her mouth and clutching a chunk of squid from her seafood dinner. The physicians examining her find what appear to be a number of tiny writhing animals stuck to her tongue, cheeks and gums. Assuming the creatures are some form of squid parasite, the medics quickly remove them.

But a closer look shows that these are no parasites: they are in fact spermatophores - tiny guided missiles containing a payload of squid sperm.

Male squid release spermatophores during mating. They then lodge themselves in the female squid’s skin near her genital opening, and release their sperm as the female lays her eggs. “Besides being a sperm package, the squid spermatophore is also an implantation device,” says José Eduardo Marian, a squid researcher at the University of São Paulo in Brazil.

Accidents will happen, though: when the Korean woman chewed on the dead male squid’s flesh she triggered the release of his spermatophores. The sperm sacs mistook the woman’s soft mouth for a female squid and implanted themselves there instead. The dead male squid had, effectively, attempted to inseminate a human female.

Welcome to the wonderfully twisted realm of sexual organs.

This is a world where penises may double as weapons during violent combat, or as lassos to snag a mate - often against her will.

It’s a world where semen can exert powerful mind control over a female, and vaginas can act to deliberately help or hinder the age-old race of sperm to egg.

And it’s a world so full of carnal conflicts of interest and deception that only now are biologists getting to grips with all of its ins and outs, including an understanding of why human sex may be about pleasure rather than pain.

The copulation armour is an organ ingeniously complicated

it is the guarantee of the preservation of the standards, the safeguard of the legitimacy of the species.

Leon Dufour [in translation]

Squid don’t as a rule attempt to inseminate humans - although with at least 16 such cases on the medical books the behaviour is more common than one might think.

But these few cases of squid-on-human action raise an important point. Our planet is populated by millions of animal species, and penetrative sex between male and female has been helping many of them reproduce for millions of years.

How do animals avoid mating with the wrong species? Leon Dufour, a nineteenth century French biologist, thought the bizarre shape of many sexual organs themselves was literally the key to the mystery.

Dufour knew more than most about the reproductive organs of insects. In 1841 he described an unusual gland in the structure some female insects use to lay their eggs - the structure has since been named in his honour.

Dufour also noticed something else during his work on insect genitalia: there is a baffling level of variety in their shape and size. So much variety, in fact, that some closely related species of insect that otherwise look identical can be distinguished purely because of differences in the shape of their sexual organs.

This doesn’t just apply to insects. A quick look at the sexual organs can help distinguish between closely related species of reptiles and mammals too. Many male mammals - although not humans - carry a bone in their penis. The variation in shape and size of this penis bone is astonishing, if a little eye watering from the female perspective.

All of this variety could be no accident, claimed Dufour, and in 1844 he came up with a theory to explain what was going on. The male of each species had developed its own, uniquely complicated sexual organ to match the equally intricate sexual organ of the female. To put it more simply, the male had developed a key to fit the female’s very specific genital lock.

Dufour’s idea implies that sexual organs double as a species recognition system: each complementary male key and female lock is so distinct that it is physically very difficult for a male and female from different species to mate. It’s a simple and plausible theory. Unfortunately, it’s also probably wrong.

There is one major flaw, according to William Eberhard of the Smithsonian Tropical Research Institute in Panama and the University of Costa Rica: female ‘locks’ simply don’t exist. The female genital tract of many species is too simple to prevent males belonging to any number of species from successfully mating with her.

This may be true, although Leigh Simmons at the University of Western Australia in Crawley points out that female genitals are generally not as well studied as male genitals, so there may be complexity there that has not been reported yet.

But if genitals have not evolved their weird shapes to act as locks and keys, then what is going on?

Penis mightier than the sword

Two flatworms face off. It’s breeding time for these simple marine animals, and that means one thing: a bout of penis fencing is on the cards.

Flatworms are hermaphrodites - animals that carry both male and female genitalia. During penis fencing, each flatworm attempts to stab the other with its two-pronged, fork-like penis. Sexual intercourse ends when one flatworm registers a successful hit on its opponent and transfers a packet of sperm.

Penis fencing is violent and a drain on a flatworm’s resources, given that some recorded fights last as long as an hour. It’s not the sort of exercise an animal would undertake without good reason.

Nico Michiels at the University of Tuebingen, Germany, says flatworms do, indeed, have a very strong motive to hone their penis-fencing skills: they would all prefer to be a father rather than a mother. With one successful penis stab to the flank of its partner, a flatworm ends its involvement in rearing the next generation, leaving it free to swim away and mate again. The stabbed flatworm, in contrast, is lumbered with all of the childcare duties.

Flatworms are an unusual case - not many animals carry both male and female genitalia at the same time. But even in species where gender is fixed, there is often a fight for the right to be father. Right at the heart of that fight you will find some extraordinarily shaped sexual organs.

The male damselfly is a classic example. Its penis - like many in the animal kingdom - is long and thin. But its tip is unusual. It carries two horn-like structures, each coated in tiny spines. These spines turn out to make a perfect brush for scrubbing away rival sperm from the female’s reproductive tract, giving the male fly a better chance of becoming a father.

Male weevils have also developed spines on their penis. But here, the spines don’t seem to be used to gently scrub away rival sperm: instead the male sinks them into the lining of the female reproductive tract during sex, apparently causing her injury. Perhaps such a harmful penis benefits the male by discouraging the female from mating with a rival in the near future - although no one has been able to confirm this with an experiment yet.

Not all males have pimped out genitalia...

Some of them rely on odd-looking sperm instead to boost their chances of fathering offspring.

The sperm of the Norway rat, for instance, have tiny hook-shaped heads that allow them to link together in their hundreds, forming a mega-sperm with several hundred tails that can power towards the eggs faster than single sperm. This gives the sperm a vital edge in the race to reach the egg before a rival’s sperm does.

Other rats play dirty. They have developed deliberately malformed ‘kamikaze’ sperm, which seem to linger behind as their peers race to the egg. These sperm are thought by some scientists to join together and form a tangled mess that ensnares the sperm of rival males - although the idea is controversial.

Even the semen that carries the sperm can help boost a male’s chances of mating success.

In many mammals - including humans - seminal fluid contains a chemical that encourages the female brain to release ovulation-inducing hormones. This may help to guarantee that there is an egg waiting for the sperm at the end of their swim. It might also help males to fertilise a female before she can mate with a rival.

Mind-bending semen seems to offer a clear advantage in the fight among males for paternity rights.

Females may not be particularly happy about being manipulated like this, though. “When we first discovered ovulation-inducing factor, we thought it may send a shiver up the spine of every woman using the "rhythm method" of contraception,” says Gregg Adams at the University of Saskatchewan in Saskatoon, Canada - although he thinks it’s unlikely that female mammals have evolved counter-adaptations to avoid this male control.

Female mammals certainly have evolved strategies to cope with other forms of male sexual control, though.

This gender conflict stems from the fact that males and females tend to have different goals in mind during mating season. It’s a quantity versus quality clash.

Males are generally keen to breed with as many females as they can: a female, in contrast, may be more interested in exploring the field and mating only with the very best males she can find. To boost their chances of getting their way, both males and females sometimes make use of some bizarrely adapted genitalia.

Gender wars

Things aren’t going well for one Argentine lake drake. His attempts to impress the female ducks with his plumage and courtship displays have failed. As yet another dissatisfied female swims away, the male instinctively reacts: in the blink of an eye he explosively releases his 40-centimetre-long penis, uses it to lasso the female and forces himself on her.

Male ducks have become notorious on the internet for what is, in our eyes, some pretty unpleasant sexual behaviour. They provide a perfect example of how the antagonistic battle of the sexes has led to some truly peculiar sexual organs - particularly because in the case of ducks, the vagina is no less bizarre than the penis.

The long duck penis is corkscrew shaped, twisting in an anti-clockwise manner. The duck vagina twists in the opposite direction, preventing the duck penis from reaching deep inside the female.

Patricia Brennan at the University of Massachusetts Amherst thinks female ducks may have evolved such a vagina to increase their level of control during the breeding season. Female ducks may tighten their vaginal muscles to thwart an unwanted male, but relax them during sex with a preferred male, making it easier for his penis to bypass the barriers and deposit sperm near to the egg. But she concedes that it won’t be easy to prove the idea. “I need a transparent duck!” she says.

Sexual conflict has probably also had a hand in shaping the strange sexual organs of the bat bug.

This close relation of the bed bug has mating habits that make even the Argentine lake duck’s look relatively tame. Males ignore the female vagina when they want to mate. Instead, they use their short, sharp penis to stab the female, injecting sperm directly into her body cavity. A female that has the misfortune to receive too much male attention can find herself at serious risk of death from the penis-inflicted wounds.

Females have responded to this aggressive male sexual behaviour by developing a special defensive structure - an area on the abdomen where the hard scaly skin is replaced by soft spongy tissue that males find easier to stab. This abdominal area focuses the attention of the male bat bug’s penis stabs. The spongy tissue is also packed full of immune cells, helping the females to avoid nasty infections that the males may pass on during sex.

But what looks like a win for both genders has actually backfired on the male bat bugs.

Females have basically endorsed the male habit of penis stabbing, and as a result males have begun enthusiastically stabbing any bat bug that strays too near – even other males.

This has become such a problem for males that they, too, have had to adapt. Some of them now sport female-like areas of spongy tissue, but the male versions are subtly different in a way that other males can apparently distinguish: male bat bugs with spongy tissue usually suffer penis-related injuries.

The final twist in this complicated tale is that females, in turn, are now taking tips from the males: the spongy tissue of some females has taken on the masculine form - a move that allows the females to masquerade as males and avoid too many penis-related injuries.

Sexual conflict has clearly helped shape some of the strangest sexual organs in the animal kingdom.

But it hasn't shaped all of them. Eberhard has looked at hundreds of insect species, and discovered something interesting: the genitalia are as complex in species that don’t resort to conflict during mating as they are in species that do. There must be one missing factor that has shaped the sexual organs.

Touching a nerve

It’s breeding time for Panama’s iridescent soldier flies. Two of the winged insects lock together in a copulatory embrace before gently spiralling downwards out of the sky to land on solid ground. Then something surprising happens. The male begins rhythmically moving his body and gently tapping the female’s abdomen. He is performing his courtship dance. Copulation is a key objective for the male fly: so why bother going to the trouble of courting the female moments after a lifetime’s ambition has been met?

Perhaps the male fly is aware that the act of copulation is not enough: if he really wants to guarantee that his genes will pass to the next generation he needs to impress his mate.

This brings us back to an earlier theme: the female is interested in mating with the best quality male she can find. She may lack the physical strength to shrug off the unwelcome advances of a poor quality male, but she can secretly reject his attempts to father her children after their brief relationship has been consummated.

In the case of the soldier fly, if a male puts on an impressive courtship display during copulation the female will often lay her eggs immediately, says Flavia Barbosa at the University of Tours in France. If the female is less than impressed with his performance, she will wait until he has finished and then fly off in search of a better male to fertilise her eggs.

It’s only within the last 20 years that biologists such as Eberhard and Barbosa have begun to realise just how much power females hold during mating. It’s easy to understand why this went unnoticed for so long: female control is often subtle and even cryptic compared to the boisterous displays of power and control often put on by males. “The studies are quite challenging to conduct,” says Barbosa.

But this cryptic female choice is now turning up almost everywhere biologists look, and it seems to have led to some peculiar sexual organs.

Female Grévy’s zebra, for instance, have ‘smart’ vaginas: the zebra can coordinate her muscular contractions in a way that flushes out the semen from a male that fails to live up to her expectations - this sperm dumping can even occur before the unfortunate male has finished dismounting.

Other female mammals have similar adaptations. If properly stimulated during sex, they can contract their vaginal muscles in a different way, this time to help transport sperm towards the eggs.

This might explain why female rabbits that have been artificially inseminated in a lab don’t allow much sperm into their fallopian tubes to fertilise their eggs. If the females are allowed to have intercourse with a sterile male rabbit just after the insemination procedure, the stimulation the male provides can make a difference: these females carry four times as much sperm in their fallopian tubes as females denied male attention.

These examples suggest that the impressive genitals that some males carry are not simply adaptations to offer him more control during mating. Instead they may owe their size and complexity to female demand.

In a sense, it’s an idea that harks back to Dufour’s 170-year-old idea of female locks and male keys. The twist, says Simmons, is that the female lock may not be physically complicated. “It could be sensory rather than morphological,” he says. The lock may only open when stimulated in a very specific way by the male key.

In other words, the female sexual organs may be a sort of sensory combination lock that the male works hard to unpick.

Penis shapes vary...

from the small and intricate, to the large and powerful

Plenty of male insects seem to have evolved unusual sexual organs solely to stimulate females - and mammals probably have too.

Despite their alarming appearance, the bizarrely shaped penis bones most male mammals carry are probably designed for pleasure, not pain. “Although we still don’t really understand what the [penis bone] is used for during copulation, I think a function in stimulating the female is much more likely than one of causing any physical harm,” says Paula Stockley at the University of Liverpool in the UK.

Men, unusually among male mammals, lack a penis bone (some scholars think the Bible may have been one of the first texts to attempt an explanation for this puzzling fact – Adam may have lost his penis bone, not a rib, in the creation of Eve). Even so, the human penis has probably also evolved to stimulate women. It is freakishly large compared to the penises of most of our closest animal relations - the chimps, gorillas and orang-utans.

Some studies suggest this is because women find well-endowed men more attractive, perhaps because larger penises offer more vaginal stimulation. This female preference may have led to a gradual increase in human penis size as our species evolved, says Geoffrey Miller at the University of New Mexico in Albuquerque.

One idea is that women, like some other mammals, use muscular contractions to retain more sperm after particularly satisfying sex, but Miller thinks it may be simpler than that.

Throughout human evolutionary history, women may just have chosen to have sex more times with the men best able to provide sexual pleasure, making it more likely that these men would father their children and pass on their genes for larger penises - particularly since humans must often have sex several times to guarantee a pregnancy. “Female humans are in the unusual position among mammals of being able to 'test' male genitalia pretty thoroughly before passing along a male's genes,” says Miller.

These latest revelations from the annals of sex research have convinced many biologists that genitalia have taken on their current shape and size to make the sexual act a more stimulating experience for the female of the species.

But probably no less convincing is the evidence that in some situations the battle between the sexes that has been the guiding hand.

Perhaps the ultimate truth is that the world of sexual organs is such a strange place because of a schizophrenic combination of both: animal genitalia evolved to make both love and war.

Photography credits:

A coloured scanning electron micrograph of a penis from a drone honeybee (Apis mellifera). During mating, a male will mount a virgin queen in the air, insert his penis and ejaculate semen. After mating, the male falls off the female leaving his penis behind. He will eventually die. Other males will continue to mate with the queen, removing the previous male's penis in the process. Credit: Power and Syred / SPL

A coloured scanning electron micrograph of a damselfly (Lschnura elegans) penis. During mating, the male damselfly uses abdominal claspers to grab the female by the neck. The female then curves her body round until the tip of her abdomen touches his genital opening and collects the sperm. The male penis has two hook-like extensions that are lined with fine hairs. These hooks are able to remove a previous mate's sperm contained within the female's sperm storage organs. Credit: Power and Syred / SPL

A scanning electron micrograph of the sexual organ of a male bedbug (Cimex lectularius). During mating, the male pierces the body wall of one of the female's abdominal segments with this organ and deposits his sperm in a sac. The sperm then migrate through the body cavity, where they are stored ready for later fertilisation. Among the insects, this so-called traumatic insemination is unique to bedbugs and related families. Credit: Power and Syred / SPL

A coloured scanning electron micrograph of a pair of bean weevils (Callosobruchus maculatus) mating. The male's penis (yellow, centre right) has a tip covered in hard spines, which unfold during copulation. These penetrate the lining of the female's genital tract, leaving puncture wounds. Mating is costly for the female (left); if she copulates with more than one male, she incurs extensive damage and so dies early. Credit: Power and Syred / SPL

A coloured scanning electron micrograph (SEM) of the tip of a male bean weevil's (Callosobruchus maculatus) penis. Credit: Power and Syred / SPL

Three female Grevy's zebras Credit: Martin Creasser / Alamy

A coloured scanning electron micrograph (SEM) of a penis extracted from the body of a flea (Ceratophyllus farrieni). The penis is normally concealed as a coil within the abdomen of the flea. During mating, the male attaches himself to the female with his antennae and genital claspers. The male is then able to uncoil his penis and penetrate the female. Mating can last from one to nine hours. Credit : Power and Syred / SPL

Southern right whales Credit: Gallo Images / Alamy

A coloured scanning electron micrograph of a fruit fly (Drosophila melanogaster) sex comb. The sex comb is found only on the front legs of males and is one of the most rapidly evolving male-specific traits in Drosophila. They use them to grasp the females' abdomen and genitalia and to spread their wings prior to copulation. Credit: Power and Syred / SPL