But are they orange?

The Universe is not only queerer than we suppose, but queerer than we can suppose

--Haldane's Law

A study was published recently on the "coevolution of male and female genital morphology in waterfowl". That is, it has long been recognized that there is a wide amount of variation in penises among those species of birds that have them. But no-one, until now, had bothered to look at the genitalia of the females of the species. The results are very interesting.

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."

Some of these elaborations included spirals in the vagina, anywhere from none to eight full 360° twists, and up to three pouches near the cloaca where sperm can be deposited, but that don't function for sperm storage.

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."

The paper is available for free on-line.

We examined vaginal and phallus anatomy in a sample of 16 waterfowl species, collected during the reproductive season. We found great variation among species in vaginal morphology. Some species had the typical simple avian vagina, whereas others had a highly complex vagina. Vaginal elaborations included a variable number of blind ending pouches proximal to the cloaca, and a variable number of clockwise spirals ending at the shell gland (or uterus). Pouches are "dead end" side cavities in the vaginal lumen that cannot be eliminated by longitudinal elongation of the vagina. Pouches are located in the distal end of the vagina, close to the cloaca, and varied in number from 0–3 among species. Spirals are full 360° twists in the vagina that can be eliminated with elongation of the oviduct, and are found at the cranial end of the vagina always ending at the shell gland. Spirals varied in number from 0–8 among species. The magnitude of vaginal elaboration we found in waterfowl is surprising because no variations in vaginal morphology have been previously reported in birds despite decades of anatomical research on avian oviducts.

Although the mechanics of copulation in birds with phalluses have not been studied, eversion of the male phallus occurs during, not prior to, cloacal contact (P. Brennan, pers. obs.). Thus, the shape and location of the vaginal pouches suggests that they might prevent the phallus from fully everting, and therefore from depositing sperm further inside the vagina. Our observations indicate that these pouches do not function in sperm storage: examination of the mucosal folds inside the vagina of Pekin duck (domestic Anas plathyrhynchos), Long-tailed duck (Clangula hyemalis), Widgeon (A. americana), Green-winged Teal (A. carolinensis) and African goose (Anser cygnoides) revealed sperm storage tubules (SSTs) only in the utero-vaginal junction, where they occur in all other avian species, and none inside the vaginal pouches. Sperm deposited in the vaginal pouches proximal to the cloaca would have a longer distance to travel to fertilize an ovum and may be more easily ejected by the female.

Congruent with previous descriptions, the phallus of all waterfowl species we examined spiralled in a counter-clockwise direction (viewed from the base of the phallus to the tip), but the vaginal spirals we discovered were coiled in the opposite direction (moving from the cloaca to the shell gland). Overall, the anatomy of these complex waterfowl vaginas suggests that pouches and spirals are anatomical barriers that function to exclude the male phallus. If this is the case, we would expect that male and female genital structures would have coevolved so that waterfowl species in which males have a longer phallus and higher levels of forced extra-pair copulations (FEPCs) would have a more elaborate vagina, while species where males have a small phallus and lower levels of FEPCs would have a simpler vagina.

A lot of people think that male and female genitalia fit together "just right", like a lock and key (or a child's toy). Unfortunately, reality isn't that nice.

Natural selection against hybridization (i.e. reinforcement) can lead to the evolution of a genital "lock and key" mechanism and complex genitalia. This hypothesis predicts coevolution between male and female genitalia because male genitalia (the key) must match female genitalia (the lock), in order for successful copulation to take place. However, since the female waterfowl vagina spirals in the opposite direction to that of the male's phallus, this suggests antagonistic rather than mutualistic coevolution that does not support the "lock and key" hypothesis.

All citations omitted.