BioEd Online

In the rough and tumble world of insect love, having a Zeus bug for a boyfriend just sucks. The girls haul the boys around on their backs for weeks at a time, feeding them all the while from a special gland located right where his royal head rests.

Why do they put up with it? Scientists now say a female shows this behaviour because if she doesn't provide her freeloading boyfriend with enough glandular treats, he's more likely to crawl up her back, lean down over her head and steal the dinner right out from under her proboscis.

The male Zeus bug violates a time-honoured tradition within the animal kingdom the male is supposed to give the female gifts, and not the other way around. Take the male spider Pisaura mirabilis, for example, which gives a gift of prey wrapped in silk, of course to distract its mate while he copulates. Or the male striped ground cricket, which allows his mate to chew on his own leg for a nourishing treat.

Males provide the gifts because they are competing for limited resources: eggs. In contrast, says ecologist Gören Arnqvist from the University of Uppsala, Sweden, getting enough sperm is rarely a problem for females. Viewed in that light, it simply doesn't make sense for the female Zeus bug to donate valuable resources to her mate.

The phenomenon is so unusual that the bugs derive their common name not from Zeus's physical stature Zeus bugs are only a couple of millimetres long but from the mythological meal the Greek god made of his first wife, Metis.

It's all give, give, give...

Female generosity could be explained if there were more females than males in the population, forcing females to compete for a suitor. "If males were a rare commodity," says Arnqvist, "then when the female finds a male, she could be willing to pay him to keep him around as a sort of living sperm bag."

But Arnqvist and his colleagues have censused wild populations of Zeus bugs and found that males outnumber females by at least 20%. In a situation like that, the males should be bringing the insect equivalent of flowers and chocolates.

To determine why females bother to feed their mates, Arnqvist's team manually sealed the gland in the back of female Zeus bugs by covering the gland with model airplane paint. They then compared the behaviour of males who were fed versus males who were left to fend for their own supper.

The group found that all males stole from their mate's dinner plate, but hungry males, deprived of treats given willingly from their mate, resorted to theft more frequently. Their results are reported in the current issue of Biology Letters.¹

... and take, take, take

John Alcock, a biologist at Arizona State University who studies insect mating behaviour, admires Arnqvist's work, but adds that there must be more to the puzzle. "The female provides the gift to protect her food," says Alcock. "But she also has to use her food to make the gift."

Arnqvist and his colleagues have suggested that perhaps the female is feeding the male cheap food that doesn't cost her much energy to make. That's possible, concedes Alcock, but wouldn't the male eventually become dissatisfied with low-quality food? "If the food is cheap, males would say 'to heck with it' and steal more of her food," says Alcock.

Bernard Crespi, an evolutionary biologist from Simon Frasier University in British Columbia, Canada, says that maybe the female is engaging in a little deception. "Those females ought to be giving him as little as possible," says Crespi. "Something that is deceptive - like junk food or something that makes you feel like you're getting more nutrients than you are."

Back in Sweden, Arnqvist's lab is already busy analysing the content of female glandular secretions to determine just how generous female Zeus bugs really are to their mates.

Visit our newsblog to read and post comments about this story.