In the world of great pond snails, receiving semen can put you in a sticky situation, as Joris Koene and his research team at VU University Amsterdam discovered.

These snails are hermaphroditic, meaning that under each nondescript brown shell, every great pond snail (Lymnaea stagnalis) carries a complete set of both male and female sex organs – like two toolboxes for different gadgets. The option to swap sexes comes in handy, but it also means that each snail must divide its resources between the two toolboxes – the more energy a snail invests in male functions (such as producing and transferring sperm) the less it can allocate to producing eggs as a female.

When two snails meet in a pond, one snail – the better-endowed one – will become the male. But it's not the size of the shell or even the penis that determines who gets the male role – it's the size of the snails' prostate glands, which produce and store semen. When a great pond snail has not mated as a male for some time and has not ejaculated, seminal fluid builds up in its prostate gland, and the gland expands. "The central nervous system gets a signal: 'It’s big!' This means [the snail] can mate as a male," Koene says.

great pond snail mating sequence_2014_05_15
The courtship stages of great pond snails. leading up to copulation (from left to right). Image: J.M. Koene & C. Levesque

The snail playing the male role will crawl onto its mate and ejaculate into it, allowing the partner to use the sperm within to fertilise its eggs. And so the romance ends, apparently without fuss … but a bit of sexual sabotage has already snuck in with the semen.

When a male great pond snail ejaculates into its partner, the semen delivers more than just sperm. The semen is a cocktail of seminal fluid proteins, two of which are covert agents that disrupt the recipient's future sperm transfer and paternity.

Disrupt how? When the snail that has been inseminated as a female goes on to mate as a male in the future, it will ejaculate with only half of the sperm count (and thus father one-fifth fewer eggs) than it would have had it not received sperm from previous mating partners.

And the snail story gets even more confusing.

Koene and his team also discovered that another seminal fluid protein, ovipostatin (which is unique to great pond snails), reduces the number of eggs laid by the inseminated snail. Limiting the number of eggs its partner produces seems to act completely against the benefit of the sperm donor … and this left Koene and his team puzzled.

great pond snail with eggs_2014_05_15
A great pond snail lays its eggs. Koene and his team discovered that the seminal fluid protein ovipostatin reduces the number of eggs laid by the inseminated snail. Image: J.M. Koene & A.W. Pieneman

Initially, Koene hypothesized that ovipostatin helped the sperm donor in unidentified ways, and that the limited egg-laying was a mere side effect of the protein. But further investigation revealed something else. It turns out that although snails that are inseminated more often (likely receiving more seminal fluid proteins) lay fewer eggs, they also invest more resources in each egg. This suggests that ovipostatin directs the partner to sacrifice egg numbers in exchange for producing better-nourished eggs.

Mating as a male and exploiting partners with seminal fluid proteins might sound like the better role by far, but there are serious perks to mating as a female as well. These snails mate and change partners frequently, receiving generous amounts of ejaculate – which they can ingest and stockpile for later use. And when no partners are available to provide sperm? The snails then simply fertilise their eggs with their own sperm, through a process known as 'selfing'.

Who knew there were so many crafty tricks hidden under the guise of those ordinary-looking brown shells?