“It is a truth universally acknowledged that a hermaphroditic flatworm in possession of its own sperm, rarely runs short of sperm, and thus must be in want of another hermaphrodite of suitable quality to inseminate.”
-Jane Austen, if she had studied flatworms

What are the economics of donating sperm? In many species where you have two sexes, male and female, the principle is pretty simple: donate sperm ALL THE TIME. Or at least as much as possible. Females tend to be more choosy about mating opportunities (due to higher eventual cost to themselves), and thus it behooves a male to get his sperm in whenever a female so much as crosses his path.

But what if both the parties involved are hermaphrodites? Well then you face something a bit different.

Vreys and Michiels. “Sperm trading by volume in a hermaphroditic flatworm with mutual penis intromission” Animal Behavior, 1998.

Hermaphrodite flatworms produce both sperm and eggs. While they could inseminate themselves and reproduce that way, what works out best is if they can donate their sperm to another worm. This means that flatworms want to get it on early and often, giving away as much sperm as possible in the hopes of inseminating, and allowing themselves to be inseminated in return. After all, if they end up with too much sperm, then they can just break it down and absorb it for food (which, I suppose, means that flatworms swallow. You’re welcome). So really, it makes sense to reciprocate, the only thing you risk is the loss of your sperm, while the gain is insemination.
(Flatworm dirty bits. You can see the ovary on one side and the seminal receptacle on the other. The penis is at the base along with the spermatophore.)

And there might also be a evolutionary signal in a flatworm letting loose a large load. In flatworms being able to produce more sperm ALSO means that you’re a very fecund female, signaling what a high quality mate you are. This would result in flatworms wants to show off their quality, and trying to give as much sperm as they get, trading equal amounts.

But do they? To figure this out, the authors of this study picked up a whole pile of mating pairs of flatworms, easy enough to find in the streams around Europe. Mating pairs of flatworms are relatively easy to get, they have long “courtship” phases where they lie flat on top of each other, inflating their spermatophores and sizing each other up, as the best matings are when the pair are the same size. Once the long foreplay period is over, each flatworm inserts a penis, and starting pumping in sperm into a sperm bladder. The sperm transfers usually start and stop at around the same time (well, flatworms work on a bit of a prolonged time scale, so within about half an hour of each other).

But the question is: are the flatworms giving as much as they get? When the authors observed the mating pairs, they showed that…well the mating flatworms were full of sperm. LOADS of it. But who’s was it? Most of the flatworms had large amounts of their own sperm as well as large amounts of sperm from other flatworms. They’ve got a ton of the stuff, so they don’t need to mate to acquire more.

So this means they are mating to give, not to get. And when they looked at pairs mating in the laboratory, they showed that the spermatophores at the end of the act were roughly the same size in each individual. They also showed that if one flatworm donated a large load, the receiving flatworm would try to match it. In other words, flatworms trade by volume, giving as good as they get. And if you get extra…well you can always break it down for food. If you’re a hot big flatworm, you’ll have a lot of sperm available, and probably a lot of eggs as well. So trading a large load of sperm is both good for you, and a good indicator that you’re a hottie to the other worm. If you’re a small sad worm on the other hand, with fewer eggs and less sperm, you can give all you’ve got, but you’ll only get so much in return, it’s not worth it to the hotter flatworm to waste more sperm on you than it’s getting. It is better to give than to receive, but only give as much as you get.

So the world of hermaphrodites is not so different from the world of two sexes. It is better to give, but you want to make sure that they can give back.

VREYS, C., & MICHIELS, N. (1998). Sperm trading by volume in a hermaphroditic flatworm with mutual penis intromission Animal Behaviour, 56 (3), 777-785 DOI: 10.1006/anbe.1998.0829