One thing you won't find in the story of the Very Hungry Caterpillar is the part where after transforming into a butterfly, he mates with a female who has a Very Hungry Reproductive Tract waiting to devour his sperm. She has a special digestive organ just for this purpose. It's so powerful that it could even compete with the gut that let the caterpillar, in his more innocent days, chew through those five oranges. This sperm-hungry organ is called the bursa copulatrix. In female butterflies and moths, it's a few zigzags away from the vagina. The sex organs of these insects are absurdly complex; a drawing of the female anatomy looks a lot like a road map. Until now, no one was sure how the bursa copulatrix—one mysterious cul-de-sac on this map—really worked. To learn more about it, University of Pittburgh graduate student Melissa Plakke turned to a common butterfly: the cabbage white, or Pieris rapae. Each female butterfly in this species can mate with many males. And this starts to explain why their sex organs are so complicated. The male butterflies, like many other insects, deliver their sperm inside a package called a spermatophore. This package can contain all kinds of goodies, such as proteins that help sperm swim quickly or plug up the female's vagina so other males can't get in. But females have their own tricks, like disabling those proteins and using them to maintain their own bodies and eggs. That means a butterfly like the cabbage white benefits from mating with many males. The more sperm packages she gets to recycle, the better. But males would prefer she restrain herself, giving each of them better odds of fathering some eggs. So they build spermatophores with tough outer envelopes. A female can't mate again until she's cleared the first spermatophore out of her system. Inside the female butterfly, sperm swim to their own storage organ while the rest of the spermatophore goes to the bursa copulatrix and gets broken down. The bursa sure looks like it's digesting this package—as a real stomach would—but scientists weren't sure how this works. So Plakke and her coauthors raised cabbage whites in the lab. They collected bursae from virgin females and from females who had recently mated. (If the females weren't virgins, the researchers carefully peeled open the bursa and tugged out the spermatophore.) Then they analyzed the bursa tissue for enzyme activity. They saw that female butterflies' bursae crank out digestive enzymes galore. "Going into the study, we had no idea whether the bursa contained a cocktail of digestive enzymes, or one main one," Plakke says. She identified nine different enzymes in the bursa that break down proteins. This is exciting, she says, because it shows female butterflies are using several types of enzymes to attack the spermatophore in different ways. The bursa is a digestive powerhouse. The researchers saw that its enzyme activity is as high as—or possibly even greater than—that in a caterpillar's gut. (Adult butterflies of this species don't eat any protein, but caterpillars do, which is why the researchers used caterpillar guts for comparison.) Yet the bursa is just one-twentieth the size of the section of caterpillar gut that digests proteins. Talk about Very Hungry. If the little caterpillar had known about the complex ways adult males and females compete with each other—a conflict so intense, it made female butterflies evolve a second stomach for their vaginas—he might have stayed inside his egg.
Image: two Pieris rapae copulating by masaki ikeda (via Wikimedia Commons)
Plakke, M., Deutsch, A., Meslin, C., Clark, N., & Morehouse, N. (2015). Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly Journal of Experimental Biology, 218 (10), 1548-1555 DOI: 10.1242/jeb.118323
