Search is on for missing pieces in puzzle of male genital diversity

PORTLAND, Ore. — Crazily diverse shapes of male genitals across the animal kingdom — from curlicues and Y-tubes to multiknobbed, tendrilly whazzits — may evolve faster than any other animal structures. Biologists have spent more than a century debating how to explain such fast and extreme variation.

Now it’s time to search for explanations in two overlooked places: the female side of sex and the vast variety of places where animals live, researchers proposed early January at the annual meeting of the Society for Integrative and Comparative Biology.

Figuring out why male genitals of a species often differ sharply from even its closest relatives’ involves basic, big ideas in biology, said Brandon Moore of Sewanee: The University of the South in Tennessee, who coorganized a symposium on genital diversity. Species arise, flourish or fail depending on whether animals mate and produce offspring or not. “This is where the rubber meets the road in Darwinian evolution,” Moore said.

Females supposedly don’t show such variety. But that notion of skimpy female diversity rests mostly on previous generations of biologists eyeballing female genitalia or taking simple measurements, said Patricia Brennan of Mount Holyoke College in South Hadley, Mass. “We like to measure length and width,” she said. But maybe what matters in male-female interactions are female structures’ curvatures, slopes and ratios.

Revisiting female anatomy with modern methods is what Sarah Mesnick of the National Oceanic and Atmospheric Administration’s Southwest Fisheries Science Center in La Jolla, Calif., and her colleagues are starting to do. Many whales and other cetacean relatives have “odd and unusual vaginal folds,” Mesnick said. A blue plastic cast of the interior cavity of a harbor porpoise vagina shows broad, slanted-sideways valleys left by the drapery of deep folds in the cavity wall. Computers can analyze variations in such hard-to-even-name shapes that plain eyeballing could miss. And more sophisticated understanding of these shapes may help explain what folds do and whether they have an evolutionary impact on male anatomy.

Modern genetics suggests that there can be strong links between his and hers shapes. For some fruit flies at least, the same gene, called Poxn,has a major influence on shape in a feature of the genitals of each sex, said Eden McQueen of the University of Pittsburgh.

Pittsburgh colleagues in the lab of Mark Rebeiz have identified a network of genes, including Poxn, that control the shape of a stout nubbin called a posterior lobe on male Drosophila genitals. By putting different versions of Poxn into otherwise genetically identical groups of flies, the researchers found that the gene controls not just a male lobe, but also the shape of the oviscapt pouch, a little pocket on female genitals. The lobe and pouch touch only briefly at the beginning of a mating. But altering their shapes changed the length of time flies actually spent copulating. 

Evolution of shape changes can get complicated under these circumstances. The best shape for the one sex may not create the best for the other. But because of the shared genes, changing one means changing the other.

Genetics isn’t the only way to look for possible links between the evolution of male and female sex organs. Michael Lough-Stevens of the University of Southern California in Los Angeles and his colleagues focused on mammals’ mystifying bones: a male’s penis bone (baculum) and a female’s clitoral bone (baubellum). What benefit they offer is unknown, said Matthew Dean, Lough-Stevens’ adviser.  

Lough-Stevens is annotating a genealogical tree with what he can find in scientific literature about which mammals do or do not have these bones. This tree may eventually give hints about what forces drove the bones’ evolution and how their histories connect.

Of the 128 species or groups on his tree so far, 111 have both bones. In gray squirrels, the male and female bones both look like asymmetric alien ice cream scoops only millimeters long. Sometimes, though, the two bones look nothing alike in the same species. Lough-Stevens showed pictures of a wavy cylinder of bone more than 60 centimeters long from a walrus penis compared with a ragged squiggle of bone only about 5 millimeters long from a walrus clitoris.  

Ten of the 128 groups have just a male’s baculum, and the rest, including humans, rabbits and hedgehogs, have neither. So far, Lough-Stevens hasn’t found mammals in which the females have a baubellum but the males have no baculum. He wonders whether lineages that lose genital bones over time tend to lose the female’s first.

Female anatomy has not been the only overlooked topic in the discussion of male genital diversity. Animals live in wildly diverse places and the demands of adapting could explain some divergent anatomy, said Brian Langerhans of North Carolina State University in Raleigh.

His recent work focuses on female fish anatomy and its links to environmental diversity, but he has found male examples, too. Gambusia mosquitofish living among predators in the Bahamas tend to grow smaller sperm-delivery organs (gonopodia) than males in safer waters. Females prefer the bigger size, but it’s a disadvantage during bursts of escape swimming.

Even human changes to the landscape can affect animal genital shape, said Justa Heinen-Kay, also at NC State and Langerhans’ student. Roadbuilding in the Bahamas has blocked off some waterways that used to connect to the sea. Male mosquitofish now living in these closed-off waters no longer contend with big predatory fish from the sea cruising in. And the tips of these mosquitofish gonopodia have widened somewhat. That change may reflect tranquil circumstances that allow males to rely more on female cooperation in transferring sperm,  Heinen-Kay and her colleagues reported in Evolutionary Applications in 2014. Thus highway planning could also join the list of overlooked sources of diversity in the mystery of male diversity.

There’s more work in progress, although meeting attendees commiserated about people who just giggle at the work instead of grappling with the big concepts. Ultimately, what may be the biggest missing factor in this line of research is widespread grasp of its weight as science.