Beyond the penis: Vaginas shaped evolutionary history
PORTLAND, OREGON—For decades, biologists have marveled at the diversity of penises across the animal kingdom—straight, forked, spiraled, spiny. But in anatomy, as in other fields, females are getting more credit. A symposium during the annual meeting of the Society for Integrative and Comparative Biology held here last week was ostensibly about the male organ. But the complexity of some female genitalia and their role in shaping phallic diversity stole the show. “Everyone feels females are the understudied sex,” says Teri Orr, a reproductive evolutionary ecologist at the University of Utah in Salt Lake City.
Even though she’s surrounded by male suitors, a female garter snake may still have some control over mating. Picture by Patricia Brennan
Researchers studying whales, snakes, and other animals are finding that female sex organs have some of the same baroque complexity seen in males. They now see females as active participants in an arms race, likely evolving more complex genitalia to help control mating and create barriers to forced matings, which in turn leads to male countermeasures. “It’s likely that female form and function drive male form and function,” says Patricia Brennan, an evolutionary biologist at Mount Holyoke College in South Hadley, Massachusetts.
Thirty years ago, the comparative evolutionary biology of intromittent
organs—penises and their equivalents—was born when evolutionary biologist William
Eberhard at the Smithsonian Tropical Research Institute in Panama drew attention to the wild variations among male genitalia. These come in all shapes and sizes, from modified anal fins to spiraling penises covered with hooks and spines. Eberhard wondered why and how this astonishing diversity had evolved. But he described the female equivalents as “relatively uniform,” a characterization that led other researchers to ignore them.
As Eberhard continued his studies of flies, wasps, and spiders, however, he began to suspect that females might be more interesting than he first thought, in part because males in so many species rub, bite, eat, or otherwise interact with females during copulation, apparently to prevent them from sabotaging the act. He also wondered whether forced copulation might prompt females to evolve defensive strategies.
That’s just what Brennan discovered in ducks in 2007. She showed that duck penises are elaborately spiraled to get into the similarly twisted vaginas of potential mates, and suggested these elaborations arose through an anatomical arms race. To combat the forced matings common in ducks and so thwart insemination by a male not of her own choosing, females evolved ever more convoluted reproductive tracts; males evolved longer penises in response. At the time, researchers considered these complicated shapes a novelty among vertebrates.
But it’s not just ducks, Sarah Mesnick reported at the meeting. Mesnick, a marine biologist at the National Oceanic and Atmospheric Administration’s Southwest Fisheries Science Center in San Diego, California, started looking at cetacean genitalia as a way of gleaning clues about the mating systems of whale populations in decline. Over the past 10 years, she, graduate student Dara Orbach at Texas A&M University, Galveston, and their colleagues have examined the vaginas of 24 whale and dolphin species by studying stranded specimens and reviewing the literature. They found internal folds that range from thin, leaflike structures to convoluted labyrinths.
The finding supports 19th century anatomists who had noted the folds, which some researchers explained as a mechanism for preventing seawater from seeping in and diluting or damaging sperm. But Mesnick and Orbach’s work, though still preliminary, argues against that hypothesis: Some dolphins have very reduced folds despite mating in saltwater, the pair reported.
During copulation, the male garter snake uses one of his spiny penises to insert a plug into his partner. Picture by Patricia Brennan
Highly convoluted folds are found in species including the harbor porpoise and bowhead whale, which have relatively large testes—often a sign that each female mates with multiple males. The researchers suggest that the folds may give females some influence over which sperm fertilize their eggs: Like the duck’s corkscrew vagina, the folds create an additional “gauntlet” that the male must navigate to mate successfully, Mesnick says.
Because researchers are unable to get a close-up view of copulations, they can only guess at the detailed mechanics of the event. In whales and even in most terrestrial vertebrates, “we have no idea how male and female genitalia interact and how those interactions affect reproductive success,” cautions Matthew Dean, an evolutionary biologist at the University of Southern California in Los Angeles. “But it’s superimportant.”
At the meeting, some researchers reported initial steps in figuring out those details. Brennan is now studying the copulatory tug-of-war in red-sided garter snakes, working with Christopher Friesen from the University of Sydney in Australia and others. In this species, males have spines at the tips of their penises, which may help them counteract a female tactic: contracting the opening of their reproductive tracts to push the penis out. As they finish copulating, male snakes deposit a plug of sperm and other material that may keep sperm from leaking out as well as prevent other males from transferring their own sperm.
The researchers removed the penile spines from some males and anesthetized the openings of some females, then allowed the snakes to mate. The plugs—a mark of male success—were much bigger in males with spines and in anesthetized females that couldn’t expel the penis, Brennan, Friesen, and colleagues reported at the meeting. Thus, the male’s spines give him an edge, one that the female counters through her contractions. “It’s absolutely critical to look at these systems as pairs,” says Diane Kelly, a vertebrate morphologist at the University of Massachusetts, Amherst.
Orr is trying to determine whether her organisms, bats, are in an arms race as well. She had been characterizing penile spines in the males, but she is now looking at females to see whether they have thicker vaginal linings in species with bigger-spined males.
As researchers delve into coevolved genital traits, they are realizing they need better ways to describe the details of the organs and the act of copulation. Dean and his colleagues have developed a grid system for pelvic bones that should provide a set of landmarks. So far they have measured the baculum, a bone in the penis of many mammals, and are beginning to describe diversity in the baubellum, a small bone in the clitoris of some mammals. The more precise measurements are helping Dean and others to better tease out the genetic underpinnings of male and female anatomy, he says.
Compared with penises, female organs are harder to map, and dissecting the intricate combination of behavior and anatomy in copulation is harder still. But Brian Langerhans, an evolutionary biologist at North Carolina State University in Raleigh, says both participants in nature’s crucial act are coming into focus. Five years from now, he predicts, “I don’t think we’ll be talking about a lack of attention on females anymore.”