Now here’s a heartwarming tale for all readers. It involves a partner who provides free transport, free food and, as a nice bonus, unlimited sex. Our story is about an insect, but it starts thousands of years ago.

According to Greek mythology, there was once a beautiful woman, the daughter of Titans, and her name was Metis. Zeus, the most powerful of all the gods, took Metis as his wife, and before long she was pregnant with the goddess Athena.

Metis was the wisest of all the gods and mortals. In Greek mythology she is the personification of deep thought and counsel. Moreover, it was prophecized that Metis would bear a child more powerful than Zeus himself. Obviously Zeus, top god though he was, felt terribly insecure about all this — and so he swallowed Metis whole. His idea was that their child would then be born through him and so thwart the prophecy.

For our purposes, the Greek myth can be seen symbolically, as a story of role reversal. When Metis is eaten by Zeus during reproduction, she is in effect feeding him (with her own body). In most species of animal, it is the male who feeds the female, either with a prey item, a nutritious secretion, or even sometimes (with praying mantis and spiders) with his own body. This makes evolutionary sense because big fatty eggs take more energy to produce than tiny skinny sperm.

But there is one insect, a water skater common along Australia’s east coast, in which it is the female who takes on the feeding role. The insect is the aptly named Zeus bug.

The male, only a millimeter long, rides around on the back of the female, feeding from her body and copulating. The Zeus bug is the only insect so far discovered where such reversed nuptial behavior has been observed. A paper on the bug appeared in Nature last month.

Usually females are choosy, and males compete to attract them, displaying bright colors or offering nuptial gifts. The Zeus bug bucks the trend of sexual selection.

“All the advantages in this relationship seem to fall to the male with no obvious advantage for the female, yet the female Zeus bug seems a willing partner in this one-sided affair,” said author Mark Elgar, a zoologist at the University of Melbourne. Elgar worked with another Melbourne zoologist, Theresa Jones, and Swedish biologist Goran Arnqvist from the University of Uppsala.

“The male can ride the female, feeding and mating for up to a week,” said Elgar. The female is about twice the size of the male, and there is a kind of “saddle” on her back where the male can comfortably sit during his piggy-back ride. Moreover, there are two glands on the female’s back that secrete a waxy, protein-rich meal for the male to snack on.

All the male has to do is lazily inseminate the female.

“The female usually produces the wax feed when a male is riding her and she will continue to produce it for as long as the male remains, yet once deposited, his sperm will allow her to continually produce batches of fertile eggs for up to two weeks,” said Elgar.

So why do females let the male stay onboard? What does the female get for continually expending precious energy to feed and transport the male?

These are questions that can’t be answered until someone (probably a Ph.D. student) has done more research. In the Nature paper, the biologists suggest that by keeping one male for long periods, possibly for the duration of her reproductive life, the female will expend less energy than she would if she tried throwing off the male after he deposited his sperm, only to have another amorous male start harassing her for a free ride.

“A constant stream of suitors wanting to participate in a polygamous free-for-all could possibly lead to greater harassment, leading to the female expending more energy and placing herself at greater risk of harm than if she doted on just the one male,” speculated Elgar.

The behavior might also have evolved to stop males cannibalizing females. The female might not want to waste that energy on feeding the male, but it’s better that he eats the secretions than eats her body.

And the male, too, has a trade-off to consider. If he leaves his saddle in search of another female, he leaves his mate open to other males in search of a free ride, so to speak.

“For the male, while it seems he may be putting all his eggs in one basket by remaining faithful, by doing so he is ensuring that his sperm rather than his rival’s sperm is being used,” Elgar said.

“The finding gives us a new perspective on how mating behaviors have evolved and been maintained.”

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