Why Most Male Spiders Castrate Themselves During Eight-Legged Acts of Love

Slate’s animal blog.
June 10 2014 1:30 PM

The Nihilistic Sex Lives of Spiders

Argiope bruennichi (Wasp Spider)
The wasp spider, Argiope bruennichi, is among the species that emasculates itself.

Photo courtesy Coussier/Flickr

Tucked away in a far corner of the northern German lowlands on the shore of the Baltic Sea, the small university town of Greifswald is a harmless vestige of Hanseatic commerce and rows of preunification apartment buildings. Its main claim to fame lies in being the birthplace of the Romantic-era painter Caspar David Friedrich. And as my old VW Beetle trundles its way along Greifswald’s access roads, snow still piled high on the sidewalks, nothing in the townscape (and certainly not the many austere Reformed Church spires), immortalized two centuries ago by Friedrich, betrays that the city is home to the hub of German genitalia research—the Greifswald Zoological Institute.

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For many years institute professor Gabriele Uhl, a charming and cheerful arachnologist, has been studying so-called mating plugs in spiders. Much to the annoyance of spider taxonomists, who need a clear view of the female genitalia for proper identification of the species, spider females’ private parts are often clogged with “dirt” or unidentifiable bits and pieces. On closer inspection, this debris often turns out to consist of male body parts—more precisely, tips of their pedipalps (a male spider’s twin penises). In a very large proportion of spiders, Uhl says, after copulation a male breaks off a part of his own genitals and leaves it behind in his mate’s. Not as an unsavory souvenir or as the result of an accident during his hasty getaway, but rather in an attempt to secure his paternity.

Spider researchers suspect that these bits of pedipalp obstruct the female’s genitalia against penetration attempts by subsequent suitors. And, says Uhl, the fact that spider females usually have separate insemination and egg-laying openings is one reason why spiders are “preadapted” for the usage of such arachnid chastity belts; after all, unlike in many other animals, the plug will not be in the way once the female starts giving birth to spiderlings. Sure enough, plugging happens everywhere in the animal world, but it proves particularly popular among spiders.

But Uhl raises her index finger and allows her eyes to twinkle. “Ah, when we say ‘plug,’ this does not mean that they are plugs,” she warns. In the black widow spider, for instance, a pedipalp tip in the female genitals does not fully prevent later males from mating with that female as well, since up to five pedipalp tips can be found lodged in a female’s genitalia. This means that the first mate’s “plug” does not dissuade numerous subsequent males from mating with the female and leaving pedipalp tips of their own. A male with broken pedipalps is effectively neutered—they never grow back—so why would males perform such acts of self-mutilation if they do not completely prevent copulation by other males? To find out the answer to this question, Uhl and her student Stefan Nessler and colleague Jutta Schneider have been studying mating plug effectiveness in the wasp spider.

The wasp spider, or Argiope bruennichi, is a striking orb-web-building spider, easily recognized by its main design feature of black and yellow cross stripes on its body as well as its habit of hanging in its webs with its eight legs held two by two in an X shape. In recent years, probably thanks to climate change, the large spider has been staging an invasion of the U.K., the Netherlands, Denmark, and northern Germany from its original stronghold in Central Europe, bringing the spectacular species more urgently to the attention of researchers like Uhl.

To work out what benefit the male gains from crowning his copulation with an act of self-neutering, Uhl and her team first visited meadows and picked almost 300 immature males and females from their webs. Letting each spider grow up in its own plastic cup in the lab, they generated a large number of mature virgin males and females. Then, in Plexiglas cages, they gave some their first sexual experience by releasing a male into the web of a female. The male wasp spider is much smaller than the female. He mates with her by crawling between her and her web and then, belly to belly, going through the ritualized motions of emptying either his right pedipalp into her right spermatheca or his left one into her left spermatheca, the whole process usually lasting only seconds. Under natural conditions, coitus then ends rather abruptly with the female sinking her fangs into the male, swiftly wrapping him in silk, and eating him. But in the lab, the researchers rescued the males by snatching them from the females’ claws as soon as his pedipalp tip had broken off and copulation was done

140610_WILD_WaspSpider-diagram

Having thus created a collection of females, some with, others without one of their insemination ducts plugged, they then turned to another batch of fresh males and proceeded to amputate one of their pedipalps to create a battalion of males with either their left or their right pedipalps missing. Now the stage was set for a clever experiment. The spiders’ mating behavior is so predictable that a male will always insert his right pedipalp in a female’s right insemination duct, and never into her left one, so the researchers could engineer sexual encounters in such a way that they could be sure that the duct a male was inserting his one remaining pedipalp into was either plugged by a previous male or still vacant. Then they measured how long the male kept his pedipalp inside the female. And since sperm is injected into the female with an ongoing pumping action, the longer the pedipalp remained inside, the more sperm was transferred.

Sure enough, the results showed that plugging the female’s genitalia, though not completely preventing a second male from mating with her, did make it harder for subsequent males to do their thing. A male forced to put his pedipalp into an already plugged insemination duct left it in there only half as long as a male ejaculating into a vacant hole. This means that to a male wasp spider, there is a benefit to leaving part of his pedipalp behind: it does not stop later males from also inserting their pedipalps, but it does hamper them in ejaculating with full force. A male that successfully plugs a female’s genitalia therefore has a higher chance of getting his just deserts than a male that doesn’t plug. And because many males do not survive their defloration anyway, they gain much but lose little by such self-emasculation.

140610_WILD_WaspSpider-cover

So, the generally poor prognosis for any male spider’s sex-life expectancy conspires with strong competition among males to produce another reason why spiders are preadapted for evolving mating plugs. Faced with such a high chance that your first time is also going to be your last, converting your genitals into a paternity-securing device is a small sacrifice given the benefits gained from protecting yourself from posthumous sperm competition.

Tidarren spiders, which twist off one of their own massive pedipalps the better to move about, are another example of spiders that have opted for plugging and self-sacrifice. Since his single remaining palp can be used only once, and since he will die a certain death in the female’s embrace, Tidarren argo uses his entire pedipalp as a mating plug. This works as follows: As soon as he has begun pumping his sperm into the female, she grabs him and twists him round and round until he gets detached from his securely fastened pedipalp, which continues to actively pump sperm into her for several hours after having been detached. As the female snacks on his body, he rests assured in the knowledge that his pedipalp will keep his sperm in and prevent other males from adding theirs. Barbara Knoflach, of the University of Innsbruck in Austria, who has been responsible for discovering many of these details about Tidarren’s bizarre sex life, ran experiments to test the effectiveness of such a plug made from a whole pedipalp. She introduced fresh males to females that had previous males’ pedipalps still stuck to their epigynes and discovered that these females tended to be barred from copulating again as long as the plugs were in place.

Tidarren has more surprises in store in the mating plug department. Knoflach discovered an even more extreme case in another species, Tidarren sisyphoides. In this species, it turns out that the male uses his entire body as a chastity belt! As soon as copulation has begun, the puny male, his oversized pedipalp happily pumping away, stiffens and dies—just like that. The female does not cannibalize him, but for hours after mating walks around with her dead lover affixed to her genitalia. Only hours later does she remove his corpse/plug and discard it.

Since in most animals males normally hope to use their genitals more than once, not many animals besides spiders have evolved mating plugs that require the amputation of parts of their penis or even of their entire penis. But there are other ways to produce a mating plug. One option: add two-component glue to your ejaculate.

From Nature’s Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us About Evolution, Biodiversity, and Ourselves by Menno Schilthuizen. Reprinted by arrangement with Viking, a member of Penguin Group (USA) LLC, a Penguin Random House company. Copyright © Menno Schilthuizen, 2014.

Nature's Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us AboutEvolution, Biodiversity, and Ourselves

Menno Schilthuizen is a research scientist at the National Museum of Natural History in Leiden, Netherlands.

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