Vagina Horrifica

It's the wet season in central Africa. The last few months have been months of plenty, but before long the threat of freezing will return, so the time to live is now. The forest is bustling with activity, animals active in the humid warmth when the heavy rains have stopped gushing down, if only for a moment. This area is a hotspot for diversity, though it pales in comparison to a proper tropical rainforest before the world froze. Maybe with time some of that diversity can be made up.

The forest breathes with the hum of life, an ebb and flow of frogs, crickets, birds, and more, intermittently split by the shrill call from whatever mammalian, amphibian, or avian throat thought it fitting to cry out. Though not contributing at all to the sound, the forest is also full of butterflies. Yes, flitting through the trees can be found myriad butterflies of every color of the rainbow, visiting flowers that are just as colorful as they. Delicately fluttering through the canopy and along the overgrown ground, they are a pleasant sight, signifying the return to familiar natural beauty despite the circumstances. Their presence is more than an aesthetic one, for each insect has its role to fill in the complicated web connecting their host plants, their preferred flowers, their predators, and their parasites.

Among these flying dancers can be found a butterfly of a specific species, and though it does not resemble any on Earth before the freeze, it is nonetheless typical, another example of the local community. It comes in two forms. One has yellow wings like sunrays, a black body covered in fuzzy white hair, and a splotch of plum red emanating from the base of its wings, which also have fine black details. The other is larger and has bright yellow wings like the first, but its red spreads much further, infiltrating the veins of its wings like spilled juice through a sponge. Its black details are more striking, too, the tips of the wings also sporting a stark white stripe.

These are splattered sunbeam butterflies, members of the pierid family of butterflies.

However, as the butterflies draw one's gaze, questions begin to appear. Visual inspection reveals that the larger, more brightly colored form is actually the female, while the male is less decorated, though certainly not dull. The female's abdomen seems greatly enlarged, perhaps explaining why she has more wing area in the back than the male. And what is with those wings, anyway, with such shape variation in a single species? Their behavior seems odd, too, for the male seems not to have time for competing with other males, always busy with other things, and the female doesn't seem to be doing much at all, sitting about in the sun with nothing to do. As the questions mount, investigation begins, and as the knowledge comes in, the idyllic image of the splattered sunbeam is forever shattered.

The shattered image is not unique to them, for some butterflies —  including pierid butterflies — have a strange and dark secret. Within each egg laid, each caterpillar hatched, and each butterfly released, a war is being fought: Not one concerning the butterflies and their host plants, their preferred flowers, their predators, or their parasites, but only themselves.

Their war is one borne initially of cooperation. Female butterflies would ordinarily have to invest their own resources into producing their eggs, as most animals do, if it weren't for a key innovation shared by all butterflies and some moths. Male butterflies, as an aid for producing offspring, produce a spermatophore for the females, a package that contains not only their sperm but a mix of nutritious chemicals. When mating, he deposits the spermatophore with his aedagus, a penis-like organ, within a pouch of hers called a bursa copulatrix, which absorbs the nutrition while the sperm break free and swim to her spermatheca to be stored for later use (For a diagram, see here). With this gift, the male can give his offspring a better chance at survival and the female can contribute less of her own resources for reproduction; a win-win for both. However, the presence of other males complicates things. Males, with their expensive nutritional gifts, would prefer that other males do not mate with females already mated with, since if that happens the female would be using some of the nutrition to grow eggs fathered by another male. They could fight each other for mating rights and often do, but it is just as viable to prevent the female from mating with other males as best as they can. In choosing this tactic, however, this puts them in conflict with the female herself, since she wants to mate with more than one male to acquire their precious spermatophores. Thus, a conflict on two fronts was born.

With time, the conflict grew into a war. Males evolved thicker coverings around their spermatophores to make the female absorb them slower and thus wait longer until she can mate again. In response, females evolved enzymes in the walls of their bursa copulatrix to break through these coverings, which caused the males to evolve thicker and harder coverings. The competition between males had become an arms race of male vs. female, and in many butterflies, this arms race progressed and progressed until it created something truly horrifying. Male spermatophores became huge, making up to 15% of their weight, and requiring so much energy that they often had to digest their internal organs and flight muscles to create when supplies were low. Coated in a tough protective layer, these enormous spermatophores are essentially 3-D printed in a many-hour process into the female. Truly startling, her bursa copulatrix has evolved from a mere pouch into a digester — nay, a stomach! This organ produces so many different types of digestive enzymes, some borrowed from stomach genes while others evolved completely anew, that they are even more effective digesters than the female's own stomach, even as a caterpillar! As the cherry on top, the digestion process requires mechanical action as well, and for this purpose females have evolved a signum — a set of internal jaws! Yes, within their bursae lies a maw lined with teeth, chewing away at the tough spermatophore as it is digested. But even this toothy maw cannot fully destroy the spermatophore's hide, so now every female carries within her the torn remains of all her past excursions.

This horrific state of affairs was the case in pierid butterflies, and the mass extinction only served to accelerate their progression. With resources suddenly scarce, it was of critical importance to ensure that they went to good use. Males competed ever harder against each other for their progeny's future while females resisted the assault to protect their progeny. Now, two million years later, the splattered sunbeams have taken these freaky mating structures to the next level. But at long last their war may be coming to an end, for the males are beginning to lose.

Viewing the bodies of the two butterflies, their progression becomes clear and the edge the female now has becomes obvious. Within the female, the bursa copulatrix has become utterly massive, running along the length of her fattened abdomen. The male's spermatophore, while also huge, is not as large, for males simply cannot keep making them larger. At up to a whopping 20% of his weight, even a well-fed male cannot produce more than one without eating at his muscles and vital organs. However, he has other adaptations to make his precious gift last as long as possible. His spermatophore is long and thin like a hot dog, forcing the female to chew away at almost the entire thing before there is space for another. To slow her even more, the inside of the spermatophore is like bubble wrap, with pockets of nutritious fluid and sperm separated by a tough membrane, so the female can no longer simply breach the wall of the spermatophore to access the innards, instead having to break every bubble. Last, he has laid in its structure chitin, the same protein that makes up their exoskeletons, providing a chemical barrier to digestion.

However, even his best efforts leave him the underdog. The bursa copulatrix's size alone is enough of a challenge, for it is so large that most females can mate again when there is still a portion of their last spermatophore being digested. Thanks to a new innovation, a female is no longer bound by the torn remains of spermatophores lying around for the rest of her life, for she is now able to expel these remains out her ovipore, the same opening that her eggs come out of. Even the spermatophore's chitinous matrix is not enough, for females have expressed a gene normally expressed in their cuticles when maintaining their chrysalis while pupating. This is the enzyme chitinase, which is able to work through the spermatophore's walls. Finally, the monster inside her has grown ever stronger.

From the muscular bursa walls protrudes the horror itself, the signum. It gouges outward with lengthy sclerotized teeth, pushing with a connected pair of discs that can invert and evert with force. It has gotten larger and heftier, with a uniquely evolved prominence the center of each disc that bears fine teeth. These bite into the spermatophore when the signum is fully everted and its discs fully splayed, removing more material with each cycle. This toothy maw is the most pivotal tool in the female's arsenal.

This near-resolution of the war between male and female dominates the lives of splattered sunbeams. Ironically, the war between males is now a quiet stalemate, a state of peace, for they will completely ignore each other unless a female is immediately present. Instead, the competition between each other manifests as the urge to collect as much food as possible, supplementing their reserves from their gluttonous days as a caterpillar. Males are smaller and built for faster, more efficient flight, and are extreme generalists, taking nectar from whatever flower their probosces can access. They also seek more atypical food sources, finding holes in plant stems, exposed fruit flesh, and fresh corpses, sucking up the sap, juice, or blood just the same. Having given up almost all combat and territoriality, they save much energy in their day-to-day lives, allowing them to invest as much as they can in their spermatophores. In preparation for mating, they may engage in an odd behavior: Rubbing their aedeagi upon clay or charcoal to cover it in the substance, aiding in neutralizing some of the female's digestive chemicals.

Females, in contrast, are lazy. Their mouthparts are very underdeveloped and their digestive tracts little more than tubes from end to end, only finding use during famine. Instead, she spends most of her time soaking up the sun in secluded areas. When ready to mate, she takes flight and gaudily shows off her wings while releasing attractive pheromones. The males, with no will to display to each other unless they both happen upon the same female, bear somewhat less colorful wings. Females are less choosy about mates than they once were, only occasionally turning down a willing male. Males, in contrast, judge their potential mates more harshly than before, for they have a hefty investment to give and do not want it to go to waste. A smaller female, or one with duller wing patterns, may be rejected. After the multi-hour mating process, he departs much lighter than he came while she retreats to rest. Here she chews and digests her meal, her dark abdomen warmed by the sun in the following days, and her eggs, now fertilized, developing within her. When the time is right she wanders off — perhaps carrying a fresher spermatophore for her next batch — and lays her numerous eggs scattered about on host plants, being able to produce many more than most other butterflies can. Borne of long-lived, heavyset mothers and short-lived, flighty fathers, these eggs have not only the challenge of survival ahead of them, but the challenge of making progress on an ancient, dying war.

And as time passes and the dust settles, they will produce something truly extraordinary.