Duelling Genitals

Although chastity belts are a fixture of the popular conception of medieval European history, scholars generally agree that there’s very little evidence they existed, let alone that they were in common use. In his book, The Medieval Chastity Belt, Professor Albrecht Classen of the University of Arizona argues that the use of chastity belts in the Middle Ages is a modern myth based on texts that were intended to be satirical or ironic. It’s as though future historians sifting through snippets of our culture came to the conclusion that UFOs throng our skies. The chastity belt myth, Classen argues, survives (and even thrives!) because it ties into prevailing notions of gender and sexual relations and feeds an ideological paradigm that contrasts the civilized (us) with the barbaric (medieval). Whatever their historical status, the biological world turns out to be replete with chastity belts and other strange genital surprises; unfortunately, as I discussed in an earlier post, our study of them seems to suffer from the same sort of ideological baggage that burdens our appreciation of history.

Mating is a delicate evolutionary game. Both players are invested in seeing a successful outcome, but the costs and risks often differ between them. Each may have the upper hand at various stages along the way — courtship, sex, and rearing — and both will try to push that advantage, possibly leading to evolution of counter-measures in a sexual evolutionary arms race. Exactly how this plays out will shape and be shaped by the species’ life history. Do individuals of either sex (or both) mate with multiple partners or is there a single, long-term pair? Or maybe there’s a pair, but also some cheating? Does one sex bear the brunt of the cost of child-rearing, either in terms of gestation or care? What about lifespan — does one sex live longer? Is food ubiquitous and plentiful or spread out in patches? All of these factors, along with many others, influence the tug of war between the two sexes in mating. One sex might be better off mating frequently and investing as little as possible in each child, while the other may have to expend more energy on the offspring and so prefer to mate less often. These conflicts of interest influence the species’ evolution, and one of their many consequences is the incredible genital morphology of animals. (Plant genitals are also pretty impressive, but that’s a subject for another time.)

Mating conflicts have led to truly remarkable adaptations in the red-backed water strider (Gerris gracilicornis). In most water strider species, the male forcibly inserts his genitals into the female’s after mounting her. Female red-backed water striders, however, have evolved a ‘genital shield’ to blocks forced entry by the males. Whereas the females of most species have exposed genitals, in G. gracilicornis the female’s genitals are mostly hidden under the exoskeleton of her last body segment. This prevents males from reaching her vulvar opening unless she extends her genitals, giving females control over the timing of copulation. Mating is more costly for female water striders than for males; as a result, females prefer to mate less frequently than males. The males’ forcible-insertion strategy allows them to mate quickly and often, but the genital shield of G. gracilicornis females enables them to slow things down and mate less frequently.

An electron microscopy image of female G. gracilicornis genitals on the left. The six panels in the upper right show the genitals in various stages from shielded (B) to exposed (G).

Faced with a highly effective lockdown, male G. gracilicornis have had to adapt by evolving a very unusual counter-strategy. After mounting the female, males don’t immediately try to insert their genitals into hers. Instead, they reach out to rhythmically tap the water with their legs, creating ripples. Although this gets the female to extend her genitals and allow the male to mate, it’s not actually a courtship signal — at least, not in the normal sense of ‘courtship’. The ripples don’t seem to be a signal of male quality to the female, but rather a threat. As their name suggests, water striders spend their time on the surface of water, and the ripples act like a beacon, lighting up the pair to underwater predators. The predators head straight for the mating couple, and the female quickly finishes mating so she can escape. It’s a pretty incredible strategy, and the males are able to get away with it because, being on top, they’re less likely than the female to become somebody’s lunch. In experiments where predators attacked mating red-backed water striders, males consistently escaped and females were consistently caught. That difference allows male G. gracilicornis to intimidate a female into mating, literally offering her a choice between copulation and death.

Duck genitals are another striking example of the twists and turns evolution takes in response to mating conflicts. Ducks form pairs during the mating season, but their fidelity is threatened by rival males, who often forcibly mate with the females. Females responded to this assault by evolving countermeasures to block access by unwanted males. The ensuing evolutionary race resulted in some of the most famous and memorable genitals of the animal kingdom. Duck penises are twisting, ballistic corkscrews that explode out of their body in a fraction of a second. Their strange shape is a response to the labyrinthine duck vagina, a convoluted collection of spirals, turns, and dead-ends. This maze is quite an effective block against unwanted matings. When a female is receptive to a male, she’ll position herself appropriately and relax her genital walls, allowing full penetration and proper ejaculation. Undesired males, however, will find their penis crashing into a wall after a wrong turn or diverted into a blind-alley, and will end up ejactulating uselessly after a partial penetration. It’s sort of an internal chastity belt, and it seems to work quite well. For the visually inclined, here’s a short video of a ballistic, twisting duck penis.

Genital shields and blind-alley vaginas aren’t all the surprises to be found in animal genitals. In some species, it’s the male that tries to block access to the female’s genitals. If females are promiscuous, males will evolve strategies to improve their sperm’s ability to compete with sperm from other matings. One approach is to use their penis to scoop out a competitor’s sperm during mating; there’s some evidence that the shape of the human penis evolved under such pressures, since it turns out that the corona (the rounded edge of the glans) is an excellent semen scooper. A surprisingly common approach is for the male to leave behind a plug to block the female’s genitals, making subsequent matings more challenging. Coagulated genital plugs are also used by spiders, scorpions, and a variety of insects, as well as rats, mice, and a variety of primates, including chimps, our closest living relatives. Male garter snakes leave behind a thick, gelatinous plug in the female's genitals, which serves as much to keep their sperm from leaking out as to stop others from getting in. In this case, the plug seems to aslo be a spermatophore -- essentially, a slow-release sperm capsule.

The medieval chastity belt may be a myth, but it turns out chastity belts of all sorts abound in the world of genital biology. Unfortunately, it seems that the field is hardly free from the constraints of our preconceptions. Biology is weird and wonderful, and it challenges us with a wealth of diversity — a fact which becomes abundantly clear from the range of genitals and mating strategies out there. Let’s strive not to be blinded by our way of doing things, whatever it may be, and not limit ourselves to a narrow, provincial view of the richness of the world.

Further reading
Brennan, PLR, et al. Coevolution of Male and Female Genital Morphology in Waterfowl. PLoS ONE 2(5): e418. (2007) doi:10.1371/journal.pone.0000418
Engle, ET. The Copulation Plug and the Accessory Genital Glands of Mammals. Journal of Mammalogy 7(2):119-126. (1926)
Friesen, C. R., et al. Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited. Biological Journal of the Linnean Society 109: 893–907. (2013) doi: 10.1111/bij.12089
Han, CS and Jablonski, PG. Female Genitalia Concealment Promotes Intimate Male Courtship in a Water Strider. PLoS ONE 4(6): e5793. (2009) doi:10.1371/journal.pone.0005793
Han, CS and Jablonski, PG. Male water striders attract predators to intimidate females into copulation. Nature Communications 1:52 (2010) doi:10.1038/ncomms1051
Shine, R, Olsson, MM, Mason, RT. Chastity belts in gartersnakes: the functional signficance of matings plugs. Biological Journal of the Linnean Society 70: 377-390 (2000) doi:10.1006/bijl.1999.0427

Image credits
The water strider image is from the paper Female Genitalia Concealment Promotes Intimate Male Courtship in a Water Strider by Han & Jablonski (2009) and is distributed under a CC-BY license.

This post is adapted and updated from an article I posted on Beacon in 2014.