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鈥檚 genital tract, wouldn鈥檛 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 G枚ran Arnqvist from the University of
Ume氓 in Sweden, that any hard evidence has emerged.
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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 鈥渨rong鈥� 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 鈥渓ocks鈥�
should diverge from one another, leading to corresponding changes in the male
genital 鈥渒eys鈥�.
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鈥攂e 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鈥� tails, are shaped by the more
subtle force of female preference, which can lead to increasingly exaggerated
male features. Darwin called this 鈥渟exual selection鈥�.
Inner knowledge
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鈥� 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鈥檚 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鈥檚 tail, you can snip bits off and
see how it affects male mating success. But with genitals, it is a different
matter. 鈥淚t鈥檚 hard to do anything manipulative,鈥� 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. 鈥淚t鈥檚 the first quantitative test of these
ideas,鈥� he says.
The rationale behind the study is simple. Post-mating sexual selection is
possible only in polyandrous species鈥攖hose 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鈥檚 idea was to compare groups of closely related species鈥攕ome
polyandrous, the others monandrous鈥攖hat 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鈥檚 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. 鈥淚n polyandrous species,
the genitalia evolve more than twice as rapidly as in the monandrous species,鈥�
says Arnqvist. What鈥檚 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. 鈥淢ost of these experiments show that when the
`wrong鈥� sperm gets in, it will fertilise the eggs,鈥� says Gwynne. But if, soon
after mating with the 鈥渨rong鈥� male, the female is allowed to mate with a male of
her own species, his sperm will fertilise the eggs. Exactly how this
鈥渃onspecific鈥� sperm always wins out is unclear. But Gwynne suspects that the
female may be getting the message from Mr Right鈥檚 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.