May 1, 2007

In Ducks, War of the Sexes Plays Out in the Evolution of Genitalia

By CARL ZIMMER

LITCHFIELD, Conn. — “This
guy’s the champion,” said Patricia Brennan, a behavioral ecologist,
leaning over the nether regions of a duck — a Meller’s duck from
Madagascar, to be specific — and carefully coaxing out his phallus.

The duck was quietly resting upside-down against the stomach of Ian
Gereg, an aviculturist here at the Livingston Ripley Waterfowl
Sanctuary. Dr. Brennan, a post-doctoral researcher at Yale University and the University of Sheffield, visits the sanctuary every two weeks to measure the phalluses of six species of ducks.

When she first visited in January, the phalluses were the size of
rice grains. Now many of them are growing rapidly. The champion phallus
from this Meller’s duck is a long, spiraling tentacle. Some ducks grow
phalluses as long as their entire body. In the fall, the genitalia will
disappear, only to reappear next spring.

The anatomy of ducks is especially bizarre considering that 97
percent of all bird species have no phallus at all. Most male birds
just deliver their sperm through an opening. Dr. Brennan is
investigating how this sexual wonder of the world came to be.

Part of the answer, she has discovered, has gone overlooked for
decades. Male ducks may have such extreme genitals because the females
do too. The birds are locked in an evolutionary struggle for
reproductive success.

Dr. Brennan was oblivious to bird phalluses until 1999. While
working in a Costa Rican forest, she observed a pair of birds called
tinamous mating. “They became unattached, and I saw this huge thing
hanging off of him,” she said. “I could not believe it. It became one
of those questions I wrote down: why do these males have this huge
phallus?”

A bird phallus is similar — but not identical — to a mammalian
penis. Most of the time it remains invisible, curled up inside a bird’s
body. During mating, however, it fills with lymphatic fluid and expands
into a long, corkscrew shape. The bird’s sperm travels on the outside
of the phallus, along a spiral-shaped groove, into the female bird.

To learn about this peculiar organ, Dr. Brennan decided she would
have to make careful dissections of male tinamous. In 2005 she traveled
to the University of Sheffield to learn the art of bird dissection from
Tim Birkhead, an evolutionary biologist. Dr. Birkhead had her practice
on some male ducks from a local farm.

Gazing at the enormous organs, she asked herself a question that apparently no one had asked before.

“So what does the female look like?” she said. “Obviously you can’t
have something like that without some place to put it in. You need a
garage to park the car.”

The lower oviduct (the equivalent of the vagina in birds) is
typically a simple tube. But when Dr. Brennan dissected some female
ducks, she discovered they had a radically different anatomy. “There
were all these weird structures, these pockets and spirals,” she said.

Somehow, generations of biologists had never noticed this anatomy
before. Pondering it, Dr. Brennan came to doubt the conventional
explanation for how duck phalluses evolved.

In some species of ducks, a female bonds for a season with a male.
But she is also harassed by other males that force her to mate. “It’s
nasty business. Females are often killed or injured,” Dr. Brennan said.

Species with more forced mating tend to have longer phalluses. That
link led some scientists to argue that the duck phallus was the result
of males’ competing with one another to fertilize eggs.

“Basically, you get a bigger phallus to put your sperm in farther than the other males,” Dr. Brennan said.

Dr. Brennan realized that scientists had made this argument without
looking at the female birds. Perhaps, she wondered, the two sexes were
coevolving, with elaborate lower oviducts driving the evolution of long
phalluses.

To test this idea, Dr. Brennan traveled to Alaska. Many species of
waterfowl breed there, with a wide range of mating systems. Working
with Kevin McCracken of the University of Alaska and his colleagues,
she caught and dissected 16 species of ducks and geese, comparing the
male and female anatomy.

If a male bird had a long phallus, the female tended to have a more
elaborate lower oviduct. And if the male had a small phallus, the
female tended to have a simple oviduct. “The correlation was incredibly
tight,” Dr. Brennan said. “When you dissected one of the birds, it was
really easy to predict what the other sex was going to look like.”

Dr. Brennan and her colleagues are publishing their study today in the journal PLOS One.

Dr. McCracken, who discovered the longest known bird phallus on an
Argentine duck in 2001, is struck by the fact that it was a woman who
discovered the complexity of female birds. “Maybe it’s the male bias we
all have,” he said. “It’s just been out there, waiting to be
discovered.”

Dr. Brennan argues that elaborate female duck anatomy evolves as a
countermeasure against aggressive males. “Once they choose a male,
they’re making the best possible choice, and that’s the male they want
siring their offspring,” she said. “They don’t want the guy flying in
from who knows where. It makes sense that they would develop a defense.”

Female ducks seem to be equipped to block the sperm of unwanted
males. Their lower oviduct is spiraled like the male phallus, for
example, but it turns in the opposite direction. Dr. Brennan suspects
that the female ducks can force sperm into one of the pockets and then
expel it. “It only makes sense as a barrier,” she said.

To support her argument, Dr. Brennan notes studies on some species
that have found that forced matings make up about a third of all
matings. Yet only 3 percent of the offspring are the result of forced
matings. “To me, it means these females are successful with this
strategy,” she said.

Dr. Brennan suspects that when the females of a species evolved
better defenses, they drove the evolution of male phalluses. “The males
have to step up to produce a longer or more flexible phallus,” she said.

Other scientists have documented a similar coevolution of genitals
in flies and other invertebrates. But Dr. Brennan’s study is the
clearest example of this arms race in vertebrates.

“It’s rare to find something so blatantly obvious in the female
anatomy,” Dr. Brennan said. “I’m sure it’s going on in other
vertebrates, but it’s probably going in ways that are more subtle and
harder to figure out.”

To test her hypothesis, Dr. Brennan plans to team up with a
biomechanics expert to build a transparent model of a female duck. She
wants to see exactly what a duck phallus does during mating.

Dr. Brennan also hopes to find more clues by studying phalluses on
living ducks. At the waterfowl sanctuary in Litchfield, she is spending
the year tracking the growth and disappearance of phalluses in ducks
and geese. Hardly anything is known about how the phallus waxes and
wanes — not to mention why.

“It may be easier to regrow it than to keep it healthy,” Dr. Brennan
said. “But those are some of the things I may be able to find out. When
you’re doing something that so little is known about, you can’t really
predict what’s going to happen.”