Siphopteron sp. 1 head injections

Siphopteron sp. 1 mating. Credit: Johanna Weminghausen

Everyone remember not to have sex with hermaphrodite sea slugs, because they'll want to inject prostate gland fluid into your forehead.

Traumatic mating is pretty common in nature. It occurs when a male uses specialised structures to wound a female, such as penis barbs in wild and domestic cats that are used to scrape the female's vagina and stimulate ovulation; or teeth in lungless salamanders that help the males keep a firm grip on the females. Often the purpose of traumatic mating is to inject sperm or other substances into certain areas on the female - called traumatic insemination - and while bed bugs are the most famous offenders, it's also been seen in a number of worms, snails, spiders and sea slugs.

With their double-barrelled penises that consist of a sperm-injecting penile bulb on one side and a syringe-like penile stylet on the other, sea slugs in the genus Siphopteron are built to inject each other with different types of fluids while they mate. Rolanda Lange from the University of Tuebingen in Germany has been studying sea slug mating habits for years, and has seen them inject each other in their feet, visceral humps (backs), and parapods, which are the pretty wing-like protrusions that run along a sea slug’s back. Working with a new species of sea slug simply known as Siphopteron sp. 1, Lange and her colleagues report a new "head injecting behaviour" in today’s edition of Proceedings of the Royal Society B: Biological Sciences.

Together with Australians Johanna Werminghausen from Monash University in Melbourne and Nils Anthes from the University of Queensland, Lange collected 32 members of Siphopteron sp. 1, which are only 2 - 4 mm long, off the coast of Lizard Island in Queensland, Australia. They were separated into eight different mating groups and allowed to mate with each other three times a day. Most of the time the mating was performed between two individuals, but there was one instance where three of them engaged in a ‘mating circle’, inseminating each other all over the place like huge creeps.

slugs intertwined

The sea slugs intertwine. Their penile stylets can be seen as the long, clear appendages directed at each other's heads. Credit: Johanna Werminghausen

Known as headshield slugs, because they plow into the sand using a strong, well-developed headshields, sea slugs in the genus Siphopteron are hermaphroditic, which means they have both male and female reproductive organs. "While there are many good theories to explain the occurrence of hermaphrodites, this is still a subject of ongoing debate,” says Lange. "In short, being a hermaphrodite, rather than a separate sex species, can be beneficial under low densities or diminishing returns to one sex function. Many species, however, simply may be hermaphrodites because their ancestors were too, and they lack some genetic ability to evolve towards being a separate sex species even if it were beneficial.”

While other Siphopteron sea slugs exhibit a pretty flexible form of hermaphroditsm, Siphopteron sp. 1 keeps things fair - everything is reciprocal when it comes to sex. So if you're a Siphopteron sp. 1 sea slug and you want to inject things into your mate's head, expect to get things injected into yours.

Having filmed 16 separate occasions of Siphopteron sp. 1 pairs mating, Lange and her team describe the process as follows:

The whole thing starts off with some romantic twirling, as the two sea slugs intertwine for around 2.5 minutes. During this stage, their penises are everted, and they'll bite each other on the back a few times. After they’re done twirling, biting and everting, the sea slugs will insert their penile bulbs into each other’s genital opening (called a gonopore), so whomever is being the 'male' can deliver his sperm. Once this is done, the pair will often explore each other's bodies with the tip of the appendage that contains the penile stylet. This tip is covered in little hair-like cilia, which could mean that it acts as a sensory organ. They will then insert the penile stylet deep into their partner’s forehead, right near the eyes, to transfer fluids that have been produced in the prostate gland. Lange refers to this head-injecting behaviour as "cephalo-traumatic secretion transfer", and this is the first time it's been witnessed in any animal species. While it sounds pretty unpleasant, Lange reported that neither member of a mating pair showed any response to being stabbed in the head, and instead remained perfectly still.

Siphopteron head injections

Siphopteron sp. 1 mating process: starting with intertwining, then reciprocal copulation, and then head injection. Credit: Rolanda Lange, Johanna Werminghausen, Nils Anthes

The forehead is not a random injection site, nor is Siphopteron sp. 1 forced to inject its mate here because that’s the only place its penile stylet can reach. In fact, it’s able to reach just about anywhere on its partner’s body, thanks to a flexible penis that can extend its entire body length. “They could reach anywhere on the mate’s body if necessary,” says Lange.

So the question is, why the forehead? While nothing’s been confirmed, and the prostate gland fluid has not yet been analysed, Lange and colleges say that it might not be a coincidence that the injection site happens to be located directly above the sea slug's central nervous system. Could they be attempting to manipulate each other on a neurophysiological level? "If there is ongoing sexual conflict in this species, ‘neural’ control of the mating partner may manipulate the recipient to behave in a way that is in the interest of the acting male not the recipient,” says Lange.

This could mean that the females, or fluid recipients, are being manipulated to store up more sperm in their specialised sperm storage organs. "Whether neural manipulation occurs in this species is at this point entirely speculative,” Lange adds. "We think that our current evidence points at it and also hope that it will spark discussion (probably also controversy) on whether or not neural manipulation of mating partners is something that generally occurs in animal kingdom, but hasn’t been looked at much."

Here's the team's video of Siphopteron sp. 1 in action:

