Photograph: Chris Draper
When it comes to male genitals, there is something
that matters a lot more than size
THE EUROPEAN RABBIT FLEA may be an obscure beast, but it does have one claim to fame: the male is widely regarded as having the most complicated genitals in the world. These are adorned with springs, levers, hooks, barbs and all sorts of twiddly bits. Here is a precision instrument that seems better suited to telling the time than depositing sperm.
Though not quite up with the rabbit flea, many other insects have some pretty impressive male genitals. Cockroaches, for example, have an articulated cluster of moving parts that resemble a Swiss army knife. And some species of dragonfly have barbed whips at the tip of their penis, while others have ominous-looking appendages, equipped with horns, that can be inflated to several times their normal size. But wherever you look in nature, from worms to mammals, you can find intromittent organs doing fair impressions of toothbrushes, nail files and other household objects.
Why are these structures so variable? If the only function of the male organ is to introduce sperm into the female's genital tract, wouldn't a simple tube be most effective? Clearly, something else must be going on. Over the years, evolutionary biologists have come up with two quite different explanations. But it is only now, thanks to a study by Göran Arnqvist from the University of Umeå in Sweden, that any hard evidence has emerged.
According to the first theory, the lock and key hypothesis, intricate genitals are species recognition devices: they evolved to prevent closely related species breeding. Because interspecies hybrids are often unfit or unviable, mating with the "wrong" species is bad news, particularly for females, who tend to invest much more time and effort in reproduction than males. So where the ranges of closely related species overlap, female genital "locks" should diverge from one another, leading to corresponding changes in the male genital "keys".
In practice, there are many instances where the lock and key hypothesis comes undone. Why, for example, have isolated island species evolved extravagant sexual organs that bear little resemblance to those of their relatives elsewhere, when there is no chance of a mating mismatch? Such anomalies have made the lock and key hypothesis fall out of favour with many evolutionary biologists. Instead, they support the theory that the diversity of male genitals is the product of competition between individuals of the same species.
It was Charles Darwin who first recognised that males who want to have their way with sexually receptive females must first win a potential mate--be it through bower building, preened plumage or ritual fighting. Characteristics such as the antlers of deer have evolved as a direct consequence of males competing for mates. Other traits, including peacocks' tails, are shaped by the more subtle force of female preference, which can lead to increasingly exaggerated male features. Darwin called this "sexual selection".
Today, many evolutionary biologists believe that sexual selection does not end with insemination. Instead, the battle may continue inside the female until the sperm of one male finally succeeds in fertilising her eggs. So as well as introducing sperm, male genitals may also be the internal equivalent of peacocks' tails or antlers, somehow increasing the chances of success for the sperm they deliver. A female may be able to exert some degree of choice over which male's sperm gets to fertilise her eggs. The intricate hooks, barbs, tufts and titillators on the male genitals might deliver internal courtship signals to the female, enabling her to assess the quality of the male.
The post-mating sexual selection theory seems persuasive, and it explains the anomalies that the lock and key hypothesis does not. But experimental evidence has been difficult to come by. With a peacock's tail, you can snip bits off and see how it affects male mating success. But with genitals, it is a different matter. "It's hard to do anything manipulative," says Arnqvist, without a hint of squeamishness.
So to test the idea, he took a new approach. Instead of doing direct experiments on individual males, Arnqvist compared the genital diversity in species with different mating habits. "It's the first quantitative test of these ideas," he says.
The rationale behind the study is simple. Post-mating sexual selection is possible only in polyandrous species--those in which females mate many times during their lives. In monandrous species, in which females typically mate only once, there is no opportunity for females to choose between the sperm of different males, or for males to oust the sperm of a rival.
Arnqvist's idea was to compare groups of closely related species--some polyandrous, the others monandrous--that shared a common ancestor. If the sexual selection idea is correct, genitals would be more diverse among the polyandrous species. But if the lock and key hypothesis underpins genital diversity, then the pattern should be reversed. Genitals would be more variable among the monandrous species because the cost of a mating mismatch will be much greater to a monandrous female than to a polyandrous female.
Arnqvist's results were conclusive. In 18 out of 19 insect groups, taken from orders as diverse as mayflies, beetles and butterflies, genital diversity was significantly greater among the polyandrous species. "In polyandrous species, the genitalia evolve more than twice as rapidly as in the monandrous species," says Arnqvist. What's more, this diversity was apparent only in genital morphology. There was no difference between the monandrous and polyandrous species in the rate of divergence of other body parts, such as wings and legs.
So is it time to throw away the lock and key? Darryl Gwynne, an evolutionary biologist from the University of Toronto, is not so sure. Although he favours the sexual selection idea, he points to some interesting experimental observations of what happens when a female mates with a male of a closely related but different species. "Most of these experiments show that when the 'wrong' sperm gets in, it will fertilise the eggs," says Gwynne. But if, soon after mating with the "wrong" male, the female is allowed to mate with a male of her own species, his sperm will fertilise the eggs. Exactly how this "conspecific" sperm always wins out is unclear. But Gwynne suspects that the female may be getting the message from Mr Right's organ. So perhaps male genitals are being used to open female locks after all, not by physically preventing interbreeding between species but by allowing females to recognise and favour sperm from males of the same species.
Whatever lingering doubts there may be, one thing is clear: for insects at least, shape matters.