Traumatic insemination - male spider pierces female's underside with needle-sharp penis

The courtship rituals of the spider Harpactea sadistica start innocently enough, with a dance and a hug. The male spider taps the female gently with his front legs and embraces her. But from that point onwards, things for the female go rapidly downhill. The male bites her and she becomes passive, allowing him to manoeuvre her into position. Like all spiders, his genitals are found next to his head, on a pair of appendages called the pedipalps. But unusually, his penis ends in a needle-sharp tip called an embolus.

The embolus sits at the end of a loop called the conductor. The male hooks one of these loops around the opposite embolus to steady it. Then, by rotating the anchored needle, he drives the point straight through the female's underside and ejaculates directly into her body cavity. On average, he does this six times, moving slowly downwards and alternating between his two penises. The entire cringeworthy sequence lasts about 15 minutes and throughout it, the male spider never penetrates the female's actual genital opening.

The species was discovered in Israel last year by Milan Rezac from the Crop Rsearch Institute in the Czech Republic. He named it well. H.sadistica practices a style of sex that's understandably known as "traumatic insemination". It's disturbingly common among insects and other invertebrates, and is most famously practiced by bedbugs. But this is the first time that the behaviour's been seen among the chelicerates - the group of animals that includes spiders, scorpions and mites.

You can see it happening in the videos below. In the first, the male spider bites and incapacitates the female. In the second, he hooks the conductor of one pedipalp around the embolus of another and, with rotating motions, drives it into the female. These videos aren't pretty - you've been warned.

When most spiders mate, the male ejects sperm into the female's vulva, and she stores it in a special pouch called the spermatheca. These pouches allow females to control when she fertilises her eggs, by voluntarily shunting sperm onto them before she lays. It also means that the last male to mate with her typically sires most of her offspring, because his sperm flushes out those of earlier liaisons.

This system means that there's a fever-pitched sperm competition between males. Different species have evolved bizarre adaptations to get an edge in these conflicts. Some guard their mates after sex. Others leave behind "mate plugs" - chastity belts that block the female's genitals. The males of one species take this to an extreme, by spontaneously dying during intercourse and turning their entire bodies into a mating plug.

But H.sadistica's brutal sexual practice allows it to bypass the competition altogether because the male's sperm can travel directly to the female's ovaries through her bloodstream. By wresting control of fertilisation from females, males ensure that when they mate, their sperm isn't shunted aside at the risk of later removal. The female's genitals support that idea, for her spemathecae have atrophied and are extremely small. Since the male doesn't ejaculate in the usual place, she has no need to keep around storage space for his sperm.

The wounds don't seem to harm the female, and Rezac never saw blood leaking from the punctures. If the females are put off by their repeated stabbings, they don't show it. Within days, they are usually ready for a new mate. It might even be positively beneficial for the female to mate with males who practice traumatic insemination. The sons of such a partnership would themselves be better at circumventing the female's sexual stores and having more offspring of their own.

It's entirely possible that in the future, the H.sadistica females will evolve a countermeasure to the male's stabbing genitals. Female bedbugs, for example, have developed a set of secondary sperm containers called 'spermalege' at the place where the males make their entries. They have effectively shunted the entire sexual process - from penetration to sperm storage - to a different part of their bodies. The original genital opening is only used to lay eggs. The same adaptations have cropped up in other insects too but H.sadistica doesn't have them... yet.

Reference:Rezac, M. (2009). The spider Harpactea sadistica: co-evolution of traumatic insemination and complex female genital morphology in spiders Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2009.0104

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