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DEEP within the darkened CAVE, the giant sperm looms. Its monstrous tail
curls around and around, snarled in a series of ferocious knots. Under an
ordinary microscope, the tangled tail would be an impenetrable blob. But here in
the Cave Automatic Virtual Environment at the National Center for Supercomputing
Applications near Chicago, a supercomputer first combines hundreds of two-dimensional
micrographs into a single three-dimensional image, and then blows it
up to the size of a Volkswagen Beetle. The sperm hangs suspended in mid-air,
like something created on the holodeck of the Starship Enterprise.

Timothy Karr, a developmental biologist at the University of Chicago, reaches
out with a computer wand to trace and measure the entire length of the sperm, or
select sections of the tail for even greater magnification so that he can
untangle its twists and turns. The sensors on his glasses tell the supercomputer
when he turns his head or walks around the image, and the computer adjusts the
perspective accordingly. It鈥檚 like some strange dream in which Karr becomes the
Incredible Shrinking Man and steps inside one of the fertilised fruit fly eggs
he studies in his laboratory.

Face to face with the giant sperm, Karr ponders a question that has been
plaguing him for years: what on earth is this sperm tail doing inside the
egg?

Sperm tend to be viewed as the biological equivalent of a rocket鈥攁
precious genetic payload, perched on top of a fuel-guzzling mechanism for
blasting it to its destination as quickly and spectacularly as possible.
Surprisingly, little is known about how the sperm and egg interact after the
moment of contact. And so entrenched is the idea of sperm as nothing more that a
convenient means of ferrying genetic cargo from male to female, that many
textbooks wrongly show the tail falling away to perish after the sperm head has
docked with the egg.

That particular misconception seems to stem from a classic text written in
1935 by the eminent biologist Julian Huxley among others. Karr, who was familiar
with the textbooks, first looked at the insides of a fertilised fruit fly egg
back in the mid-1980s. He was amazed by what he saw.

鈥淚 had discovered a giant piece of spaghetti inside the egg,鈥� he says. 鈥淚
just said, `What鈥檚 this?鈥� I had no idea.鈥� But it wasn鈥檛 spaghetti. It was a
whole sperm, tail and all.

The tail of a sperm is formed from specialised microtubules, protein
cylinders that make up the propulsion mechanism. Karr had used a fluorescent
stain to highlight the intended object of his interest, the proteins of the
egg鈥檚 cytoskeleton, and his stain serendipitously lit up the sperm鈥檚 microtubule
proteins as well.

Fruit fly sperm aren鈥檛 just gigantic because of the magnification in the
CAVE. They can be truly huge鈥攁t least when compared to a diminutive
1.5-millimetre fruit fly. The length varies from species to species but in some
the sperm, when laid out straight, are more than 20 times the length of the
fly鈥檚 entire body. Karr had discovered that massive structure crammed into one
end of the fruit fly egg. And he was intent on finding out exactly what a sperm
tail, giant or otherwise, might be doing there.

Karr鈥檚 next surprise was that the sperm tail seems to persist pretty much
intact throughout embryonic development. Both sperm and eggs contain
mitochondria, tiny organelles that generate energy for the cells. But while the
offspring of fruit flies, humans, or any other animal species inherit all their
mitochondria from their mothers, fathers keep their mitochondria to themselves.
In humans and other mammals, the sperm tail and its mitochondria are thought to
be degraded by enzymes very early in embryonic development. At some point the
fruit fly embryo must also dispose of its sperm tail. But when and how? wondered
Karr.

Winged testes

From the very beginning, Karr had some ideas about what the intact sperm
might be doing in the egg. Perhaps the tail helped line up the egg and sperm
nuclei before they fused. Or given its size and the fact that it always sat at
the anterior end of the egg, perhaps it elicited some physical or chemical
perturbations that marked the front-back axis of the embryo, a key stage in the
development of any animal.

All that was just speculation. Still, Karr reasoned, the presence of the
sperm tail in the very same place in every egg suggested that biologists had
overlooked something important in the development of fruit flies and perhaps
other species too. Others disagreed. Some people 鈥渆ven suggested that I was
crazy鈥�, says Karr. 鈥淚t was a lonely period.鈥�

Then, a few years ago, Karr got a call from Scott Pitnick, an evolutionary
biologist at Syracuse University in New York. 鈥淗e basically talked my ear off
for a couple of hours,鈥� says Karr. 鈥淚 didn鈥檛 know what he was talking about. I
hadn鈥檛 considered evolution or ecology or any of those things.鈥�

Pitnick has been fascinated with giant sperm and the anomaly they represent
ever since his student days. And while Karr wanted to know what a sperm tail
from a fruit fly or any other species might do in an egg, Pitnick wanted to know
why the fruit fly sperm had got so big. 鈥淔ruit flies with giant sperm are
basically testes with wings,鈥� he says.

Take Drosophila bifurca. Each sperm is 6 centimetres long, and its
testes take up half of its abdominal cavity. Usually the males of a species
produce hundreds of tiny, throwaway gametes, and it鈥檚 the females who invest
their resources in relatively few, large gametes鈥攑icture a lone, hulking
egg swarmed by millions of stampeding sperm. But in the fruit fly, it鈥檚 the
males who invest resources in their sex cells, and then use them sparingly.

D. bifurca dedicate 17 days to making their sperm鈥攁 long time
for a fruit fly that only lives for a few months. The females, in contrast, get
down to business when they are 7 days old. 鈥淢ales spend half of their lives in a
non-reproductive state! Why not produce lots of tiny sperm and start reproducing
immediately?鈥� Pitnick asks. 鈥淭hat鈥檚 the big question.鈥� And D. bifurca
is not alone. The males of other fruit fly species also wait a long time before
having sex, presumably because they, too, are lavishing resources on the
production of impressive gametes.

Male fruit flies can also be extremely pernickety about how they handle their
prize sperm once they鈥檝e made them. In most fruit fly species, the long sperm
get presented to the female as a mixed-up jumble, so huge that it鈥檚 visible to
the naked eye. But the male D. bifurca uses his spiralling genital duct
to roll individual sperm into pellets, and then line up the pellets in single
file, according to a study by Dominique Joly and her colleagues at France鈥檚
national Population, Genetics, and Evolution laboratory in Gif-sur-Yvette (
Nature, vol 377, p 202). The long sperm tails make swimming
impossible鈥攊magine trying to flap a mile-long piece of damp
string鈥攕o during sex (Joly has timed it; copulation takes on average 374
seconds) the male uses the tip of its genital duct to carefully deposit a mere
20 or so sperm pellets into the female鈥檚 uterus. Once there, the sperm are in
for a shock.

Just as sperm are usually depicted as comic-book heroes, the egg is usually
seen as a single-celled Sleeping Beauty, languishing at one end of a long,
obstacle-ridden reproductive tract. In fact, in most species, both the egg and
the female reproductive tract play an active role in engineering fertilisation.
But once again, the fruit fly goes to extremes.

Hansel and Gretel

The female somehow hauls the helpless sperm pellets into a large holding cell
where the uterus joins the oviduct. Then a chimney-like tube at one end of her
egg lines up with the entrance to this cell, and appears to suck in the giant
sperm.

What evolutionary pressure could possibly have produced these ridiculously
large, doltish sperm? Pitnick had a handful of theories. Perhaps the long tails
somehow help sperm beat the competition when it鈥檚 time to leave the cramped
confines of the females鈥� holding cell. Or perhaps the females鈥� genital tracts
favour long sperm tails in much the same way that some biologists argue that a
peahen likes the peacock鈥檚 glorious tail鈥攏ot because it鈥檚 useful, but
because it signifies some other genetic trait that will benefit the embryo鈥檚
survival or its reproductive success. Or perhaps the sperm helps nourish the
developing embryo鈥攖he longer the tail, the more nourishment; the more
nourishment, the more likely the embryo is to survive, and the sperm to pass on
its genes. Pitnick and Karr have managed to strike at least one of the options
off the list, using the virtual reality CAVE.

Viewed in two dimensions, or even on a computer screen in three dimensions,
the sperm tails are so jumbled up it鈥檚 impossible to tell which stretch of tail
goes in front of another, or how all the loops are connected. But it all becomes
clear in the CAVE. Working with 鈥淐AVE queen鈥� Rachael Brady, and her virtual
reality software CRUMBS, Karr dropped computerised markers along the sperm tails
to keep himself from getting lost in their snarls, much like Hansel and Gretel
used breadcrumbs to mark their path. His trail revealed that not all of the
sperm tail disappears into the egg in every species of fruit fly. And the longer
the tail, the more tends to get left out in the cold. For example, D.
bifurca鈥檚 egg accepts only 1.60 millimetres of the sperm鈥檚 enormous
6-centimetre tail, while D. pseudoobscura eggs take in the full 0.36
millimetres of their relatively short sperm tails. When Karr and Pitnick plotted
total tail length and length of tail inside the egg for 12 fruit fly species on
an evolutionary family tree (Nature, vol 379, p 405), a pattern
emerged.

The ancestral fruit fly species appear to have had shorter sperm that fully
entered the egg. Some later species have evolved longer and longer sperm
tails鈥攄espite the fact that in some of those species the eggs summarily
cut off the sperm tail so that only a tiny fragment got in. Clearly, if large
parts of the tail are left outside the egg, it isn鈥檛 the sperm鈥檚 ability to
nourish the egg that drives the evolution of giant sperm, reasons Pitnick. The
two researchers even have preliminary evidence that the egg is running the show,
drawing in the sperm like someone sucking up a piece of spaghetti until it has
just the right amount for its species. The sucking force could come from the
shifting of cytoplasm within the egg, Pitnick speculates.

While Pitnick and Karr may not yet know why the giant sperm have evolved,
they now have good evidence that it is doing something important in the
developing embryo. After poring over data from Karr鈥檚 days spent locked up in
the CAVE with giant sperm, the two researchers have come to some startling
conclusions. Rather than taking on any old shape, the sperm consistently forms a
recognisable structure in the egg, suggesting a specific function. What鈥檚 more,
the shape of that structure is completely species-dependent.

鈥淚 can show Tim [a CAVE image of] a fertilised egg and he can tell me what
species it is just by eyeballing it,鈥� Pitnick says. Earlier he had discovered
that fruit fly sperm length evolves extremely rapidly鈥攃losely related
species can have sperm lengths that vary by an order of magnitude鈥攈inting
that the sperm tail might be part of a previously unidentified mechanism for
creating new species. Finding that the sperm shape in the egg was
species-dependent just fuelled Pitnick鈥檚 suspicion.

Fruit flies are particularly good creatures in which to study the mysterious
process by which new species are made. Although there are technically thousands
of different fruit fly species, many of them dwell in the grey fuzzy area
devoted to species that have yet to become truly isolated. Some fruit fly
species can mate, but would never encounter each other in the real world. Put
them in a test tube and play some mood music, however, and they鈥檒l get it on.
Usually their offspring are infertile, much like the offspring of a donkey and a
horse, but sometimes they produce seemingly normal fruit flies.

For new species to develop, groups of plants or animals must be isolated so
that the gene flow between them stops, and they evolve separately. The isolation
can be purely geographic鈥攊f the animals or plants get separated when one
land mass breaks away from another. Or it can be behavioural鈥攊f one group
of a particular species develops a new mating dance that baffles outsiders. Or
it can be physical鈥攐ne group is no longer anatomically equipped to mate or
to create viable offspring with another group of the same species. Pitnick and
Karr suspect that the rapidly evolving sperm could create just such a physical
barrier between would-be new species, perhaps by playing some vital role in
embryo development.

Maggot poop

To test that theory, Karr and Pitnick are now crossing fruit flies that are
from different species, but still capable of mating when put in close contact,
and using the CAVE to see if the resulting embryos are normal. The next step is
to shear off part of the sperm tail, and then inject the sperm into the uterus
of a female of the same species. If the embryo fails to develop normally, that
would be yet more evidence that the sperm tail plays an essential role in
embryonic development.

Sperm-egg interactions after fertilisation are 鈥済oing to be a very fertile
area in understanding speciation and developmental biology,鈥� predicts Pitnick.
鈥淚t鈥檚 been sorely neglected.鈥�

Meanwhile, biologists at sperm meetings are fascinated by Karr and Pitnick鈥檚
research, if ultimately baffled about what conclusions to draw. 鈥淭he research is
so mind-boggling it really makes people sit up and take notice,鈥� says Timothy
Birkhead of the University of Sheffield, who organises a sperm conference every
other year. 鈥淭he technology they鈥檝e used, the virtual reality to get inside the
egg, is surreal. But the basic phenomenon [of giant sperm] is still a
尘测蝉迟别谤测.鈥�

But there is one giant sperm riddle that Karr and Pitnick have
solved鈥攖he mysterious fate of those sperm mitochondria. This is what
happens. Soon after the sperm enters the egg, and just as the egg is being laid,
the embryo nucleus divides rapidly at one end of the cell, while the sperm tail
lurks at the other. Around the seventh or eighth cycle of nuclear divisions, the
nuclei suddenly migrate to the periphery of the embryo. A thousand nuclei line
up all around the outer edge of the embryo, with a few falling back into the
middle. Then, cell membranes form around the nuclei, leaving a large open area
in the middle of the embryo. This is where the sperm tail sits.

Development continues. The middle of the embryo becomes the gut, a gut with a
sperm tail sitting in it. Little fruit fly maggots are hatched. And those little
maggots 鈥減oop out the mitochondria,鈥� says Karr, who will publish the findings in
the 7 May issue of the Proceedings of the Royal Society of
London鈥擲eries B.

Karr notes that the egg could have used enzymes to chew the whole thing up.
鈥淏ut that鈥檚 not the way it decided to handle this giant structure,鈥� he says.
鈥淧erhaps it better to throw something out in the garbage than to tear it up in
your living room?鈥�

Or perhaps, he says, it鈥檚 just one more sign that the sperm tail, far from
being a piece of mitochondrial-laden junk fit only to be discarded at
fertilisation, is in fact playing some essential, if mysterious, role in the new
embryo鈥檚 development.