Enlarge /. Look closely into the spider's two largest eyes and you can see internal structures that are similar to those we developed.
First, the confession: I am an arachnophobic who is frightened by the most harmless everyday spiders. Close encounters with the more scary strain – the goliath bird-eating spider in a college student zoology class, the venomous redback who share my tent on a research trip to Australia – let's just say they taught me more about myself than about arachnids. Yet I've discovered a soft spot for a group of spiders: those undersized men who are faced with the daunting prospect of having sex with a giant partner, often facing murder. Think of the 50-foot woman's attack, just with spiders.
Why the compassion? It's not because these puny men risk their lives for love. That's because they came up with such bizarre ways to achieve their ultimate goal of conceiving spiders with a mother's monster.
The dimorphism of sexual size – where one sex is larger than the other – is nothing out of the ordinary: imagine a massive male orangutan or the bull elephant perched above his harem. And many insects and other terrestrial arthropods have large females because a larger body can produce more eggs.
However, spiders beat all comers: women can be three to ten times the size of men, and occasionally more. Most of these mismatched pairs are web-spinning spiders, particularly orb weavers and widows. Female giant golden ball weavers (Nephila pilipes), for example, are ten times as long as males and 125 times heavier.
Welcome to the world of eSSD – extreme dimorphism of sexual size.
Such spectacular discrepancies have consequences, and the most notorious of all is cannibalism. Giant female spiders sitting in their webs waiting to be courted are the definition of femmes fatales, who tend to nibble on their suitors before, during, or after copulation. Why? Because they are big and can do it, they not only get a reasonably decent dinner, they also control who is lucky and who is not.
Less known is the amazing repertoire of male behavior in these species, all of which are aimed at enhancing fatherhood. While women are just waiting, men have to go around looking for partners. If they find one, they may need to fend off rivals, don't need to be eaten long enough to mate, and try to stop other males from impregnating the female after they're done. And that has resulted in amazing tactics.
“Sex with animals can be weird, but it's really weird. It's like a soap opera, ”says arachnologist Jonathan Coddington. As a curator for arachnids at the Smithsonian's National Museum of Natural History in Washington, DC, he has spent decades studying the evolution of spiders and observing their strange sexual habits.
Spider sex is unique even if extreme differences in size are ignored. Mature men squirt their sperm onto a tiny "sperm web" and then suck the sperm up into attachments on the sides of the head for storage until mating. In women, these appendages – called pedipalps – are leg-like structures that are used to poke and examine prey. In men, however, the tips are converted into sperm organs.
During copulation, the male inserts a palpus into an opening in the female's abdomen and pumps in sperm. When given the chance, he will insert his second palp into the female's other opening. There, his sperm – and that of a later successful man – is kept in bags called sperm libraries until the female begins to lay eggs. At this point the sperm are activated, migrate into the egg-laying channel and fertilize the eggs.
This process presents some difficult challenges for odd partners, but before reaching conclusions, ill-fitting sex organs are not one of them. "Evolution has made sure that the genitals of gigantic women are relatively small and the smaller men are relatively large," explains the Slovenian spider specialist Matjaž Kuntner from the National Institute of Biology in Ljubljana. A bigger problem is surviving long enough to stop copulation and fertilize all or most of the woman's eggs.
Take precautionary measures
Male ball weavers approach with caution from behind, keeping as far away from female jaws as possible. In many species, males choose a time of least danger when given the chance: when the female is already eating or when she molt for the last time before adulthood. Moulting women cannot attack until their soft new exoskeletons harden.
The German zoologist Gabriele Uhl from the University of Greifswald examined how well this strategy serves the black and yellow striped wasp spider (Argiope bruennichi). In laboratory studies, 97 percent of the men who mated with the soft, molting women survived, compared with 20 percent who tried to mate with a hardened one. In addition, mating a still soft woman allowed the men to copulate longer and gave them the option to empty both palps or try their luck with a second partner.
In her study, Uhl estimated that around 45 percent of the wasp spider males mated with molting females. It is difficult to know how common this tactic is in other spiders because the moulting is quick and often at night. "The researchers would have to stay up all night to observe it," says Uhl. She believes this is widespread, however, as males of many species are known to hang in and around the nets of immature females. And it's a tactic that pays off, she says. "It is very likely that males who mate with molt pairs will all father their offspring."
Some male spiders resort to calming gestures when threatened. If the female giant golden ball-weaver breaks the pairing (a bad sign), the male ties her with silk threads. The bonds aren't strong enough to immobilize them, but the caress relaxes them enough to resume mating. This could also explain why Darwin's bark spider (Caerostris darwini) performs oral sex and salivates on the woman's genitals before copulation. This recently discovered behavior has only been observed in this particular species of spider, but researchers suspect it could be widespread.
And then there is the sensible, if impossible-sounding strategy of remote copulation. That doesn't seem to be quite the case, as the Asiatic recluse spider (Nephilengys malabarensis) shows. When danger threatens, the male snaps off his pedipalps and does his escape well, allowing the palms of his hands to pump sperm without him.
So far, so bizarre. But that is not all. The evolutionary interests of men and women are not always alike, which makes sex a battlefield in several ways. His interest lies in the transmission of his genes, so he benefits from fathering all of his partner's offspring. For the woman, monogamy isn't such a good idea: she wants offspring with the best possible genes so she can either be picky or mate with multiple males, which increases the likelihood that some of her spiders will get good.
This conflict has resulted in each gender developing measures and countermeasures to achieve what it wants. Women eat men they don't want to mate with or who don't want to be monopolized by a single partner. Men have found ways to thwart women. "For men, the chances of finding a second woman to mate with are virtually nil. That's why he invests everything in being successful with a partner – and that has led to a lot of bizarre behaviors," Coddington says.
For example, men often gather on one woman's net where they struggle to come first to try their luck. Successful men try to ensure paternity by preventing rivals from giving their sperm to their store. You can try closing off the woman's copulation openings by leaving the ends of her palms or even entire palms behind. Even then, and assuming that they survived the mating, they often jealously guard the woman and fight to fend off other suitors. Asian recluse spiders that complete copulation without fleeing halfway and doing the work remotely still leave their palms behind when they're done. A study from Kuntner's lab showed that 87 percent of them left their palms this way, chewing them off when needed. The team also showed that these “eunuch” men are more agile, superior fighters who can better protect their partner.
However, not all genital plugs work, as Coddington has endeavored to point out. The pedipalps of the huge golden ball weaver end in long, hair-like extensions. “He puts it in the female; it breaks off and doesn't do anything, ”says Coddington. "We find women with eight or more stuck in them."