A Reproductive Arms Race Between Duck Sexes

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An interesting article was published today by a group led by Patricia Brennan in the open-access journal, PLoS One, about the structural co-evolution of duck phalluses and vaginas. What, you ask? Ducks have phalluses? Yes, indeed they do. Further, ducks are also famous for forced copulations -- as many as 30% of all copulations are forced -- so it only makes evolutionary sense that females have co-evolved a method for excluding sperm they don't want fertilizing their precious eggs.

This paper examines the reproductive and evolutionary arms race between male and female ducks to control paternity. Basically, if males develop large and elaborate genital structures that allow them to manipulate females and to bias paternity in their favor, then females will co-evolve specific genital anatomy that allows them to regain some control over copulation and/or fertilization success -- so females can exercise choice over which male fertilizes their eggs.

"Basically, you get a bigger phallus to put your sperm in farther than the other males," Brennan said. Essentially, this phallus functions to deposit semen closer to the site of sperm storage and/or fertilization and increases their likelihood of fertilization, thus providing males with a copulatory advantage over females.

But the problem was that scientists had not looked at female ducks' anatomy, so they were arguing their point strictly from a male perspective. In the case of ducks, males have a phallus that varies from an inch in length to the length of the entire body.

"So what does the female look like?" Brennan asked. "Obviously you can't have something like that without some place to put it in. You need a garage to park the car."

As a result of her studies, Brennan and her colleagues found that, 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," said Brennan. "When you dissected one of the birds, it was really easy to predict what the other sex was going to look like."

For example, the phallus of all waterfowl species examined were spiralled in a counter-clockwise direction, whereas the vaginal spirals were coiled in the opposite direction. As a result, the anatomy of complex waterfowl vaginas suggests that pouches and spirals are anatomical barriers that exclude the male phallus.

The team hypothesize that male and female genital structures coevolved so that waterfowl species in which males have a longer phallus and higher levels of forced extra-pair copulations (FEPCs) would also have a more elaborate vagina, while species where males have a small phallus and lower levels of FEPCs would have a simpler vagina. All this, so each female can retain control over who fertilizes her eggs.

"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."

To support her argument, Brennan notes that in some species, forced matings make up about a third of all matings, yet only 3 percent of the offspring result from these forced pairings.

"To me, it means these females are successful with this strategy," she observed.

The group's phylogenetic analysis of phallus length evolution in their sample of 16 waterfowl species indicated that large phallus size evolved independently and convergently in at least three lineages: stiff-tailed ducks (e.g. Oxyura), dabbling ducks (e.g. Anas) and diving ducks (e.g. Clangula). Furthermore, all three of these lineages show correlated evolution of anatomical counter-measures in the female reproductive tract.

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," 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."

According the the NYTimes piece, Brennan is currently studying phalluses on living ducks by 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. Well, as an aside, I can say that my dissertation research showed that the enlargement of the cloacal protuberance in white-crowned sparrows is a endocrinological event: seasonally increasing levels of testosterone and androgen receptors in cloacal tissue results in an enlarged cloacal protuberance, whereas falling hormone levels cause the cloacal protuberance to diminish. The cloacal protuberance is similar in function to a duck phallus, so perhaps similar endocrinological events occur in ducks on a seasonal basis?

Sources

Original article: Coevolution of Male and Female Genital Morphology in Waterfowl by Patricia L.R. Brennan, Richard O. Prum, Kevin G. McCracken, Michael D. Sorenson, Robert E. Wilson, Tim R. Birkhead PLoS One [article]

NYTimes (quotes)

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