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Thursday, June 26, 2003

NATURAL SELECTIONS

Hard-core S&M sex . . . on the web


In 1996 Cosmopolitan magazine ran a humorous piece about men who had died during sex. One of the most famous cases is that of the former French President Felix Faure.

In 1899 Faure was being entertained by his mistress, Madame Steinheil, when he suffered a fatal heart attack. Legend has it that he died of apoplexy, that is, of a cerebral stroke caused by a brain hemorrhage. Another tale tells of how Steinheil was so shocked when Faure died that she suffered lock jaw and had to be pried from the stiff presidential member at the hospital.

Men will risk much for sexual gratification. And, as regular readers of this column will know, males of other species go to all sorts of extremes to fertilize the eggs of a female. Bedbugs hack directly through the female's body wall to gain direct access to the ovaries. Male praying mantises will allow themselves to be decapitated and eaten as they copulate.

But this week we have an animal that goes further still -- and recalls the dark end suffered by Faure.

The orb-weaving spider Argiope aurantia makes things so easy for the female you have to wonder if he'll be voted the ideal male by the editors of Cosmo: He dies during copulation.

Sexual cannibalism is well-known in spiders. In many species, the female devours the male during or after sex. Just as sperm are to eggs, male spiders are tiny compared to the female. A female A. aurantia may weigh 50 times more than the male, so she is unlikely to get much of a meal from him, but she'll eat him anyway.

Usually, male spiders approach the female with extreme caution and, if they are successful in mating, try to escape from her hungry jaws afterward. In these (indeed, in most) cases of sexual cannibalism, males get a raw deal. It would be better for them to stay alive to copulate another day.

Male redback spiders, however, basically commit suicide by enticing the female to eat them. If the male is consumed during mating he stays attached to her for longer -- and thus fertilizes more eggs. So what of the orb-weaving spiders who die during sex? Who die, in fact, at the moment of penetration?

Zoologists Matthias Foellmer and Daphne Fairbairn of the University of California, Riverside, heard reports about this and decided to investigate. Their results are published this week in the Royal Society journal Biology Letters.

Male A. aurantia spiders mate in one of two ways. They either find an immature female, and wait until she molts into her mature form, at which point they copulate with her. The just-molted female is soft and defenseless and such copulations are referred to as "opportunistic." The other method is to find a mature female and court her. If she accepts the male's advances, he can then mate with her.

Male spiders don't have a penis, but a pair of organs called pedipalps, which serve as the copulatory structures.

The pedipalps are filled with sperm from the testes, and the spider must insert them into the female's paired genital openings. Upon insertion, the palps are inflated and sperm is transferred.

Foellmer and Fairbairn watched spiders in the field and in the lab, and found that during opportunistic matings (those with just-molted females), once both pedipalps were inserted, the males died, with their legs curled stiff and motionless under the body. The soft-bodied females were unable to dislodge the dead male for at least half an hour.

When males approached mature females, they tried to escape after inserting the first pedipalp. Probably they prefer to mate with a just-molted female, so are willing to settle for only one pedipalp, and thus, only one of the female's sperm stores. But as soon as they inserted the second pedipalp, they curled up and died. Mature females, whose bodies are hardened, have no trouble quickly pulling the dead male from their bodies (and consuming him).

The researchers confirmed (by examining males' bodies under a microscope) that the heartbeat ceases within minutes of pedipalp insertion. And in a freak observation, Foellmer and Fairbairn saw a male spider insert his pedipalps not into a female spider, but into the carcass of a beetle larva caught in the web. He too, instantly died.

It is difficult to show the benefit to males of such an extreme outcome to copulation, since all males appear to have the same response. If some males survived, the scientists could compare their reproductive success to those who died at copulation. But given that they all died, why is it that this programmed death evolved?

"Terminal reproductive investment is expected to evolve when the benefits of this investment outweigh the cost of foregoing future mating opportunities," the authors write.

A benefit might be that the female eats the male and the meal enables her to lay more eggs (which his sperm fertilize). But we have already seen that such a small meal is unlikely to be of much use to the female.

Alternatively, by dying while still attached to the just-molted female, the males may prevent other males from displacing them. Many male insects use a mating plug after sex -- a kind of chastity belt that prevents other males from going where they've just been. Could this be the case with the orb-weaving spider?

"Because the palps of dead males are fixed in the inflated state and are therefore harder to remove, dead males act as whole-body mating plugs, often preventing other males from mating," write Foellmer and Fairbairn.

As the mistress of the late president of France found out, dead males maintain an "inflated state" and can be difficult to dislodge.

"Pulling out a dead male with forceps requires some force and often the female is pulled along off the web!" said Foellmer via e-mail.

The work suggests that orb-weaving spiders mating just-molted females can benefit from spontaneously dying during sex.

Rowan Hooper welcomes comments at rowan.hooper@tcd.ie


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