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CALIFORNIA WILD

FEATURE STORY

Material Girls

Maggie McKee

As animal totems go, penguins take their place somewhere between the regal eagles and the hapless hippos. By virtue of their sleek lines, “formal” wear, and pure exotic appeal, penguins symbolize dignity and class. But their decidedly awkward waddles and round, fuzzy offspring also make them adorable and endearing.

So it might come as a surprise that, at times, penguins behave in ways that seem neither stately nor cute but, well, sleazy. To wit, Adelie penguins regularly steal stones from fellow nest-builders to fortify their own, even though they get pecked and chased in the process. More surprising yet is the recent discovery that some females resort to peddling their bodies in exchange for the precious pebbles.

And penguins are not the only creatures to exchange sex for a material benefit (aside, of course, from humans). A few other birds trade sexual favors for food, and many insects have evolved elaborate quid pro quo sexual arrangements. In several cases, one or another of the individuals involved has even figured out a way to get something for nothing.

Animal behaviorists believe these deals could have evolved for several reasons: to encourage sex; to provide a kind of child support for the third party’s potential progeny; or to lay the groundwork for a possible future relationship. In any case, with some of the examples stretching back millions of years, prostitution seems to live up to its reputation as the oldest profession.

For Adelie penguins in Antarctica, that could be modified to the coldest profession.

Every year around the end of October, about two million of these birds, who spend most of their lives in the ocean, trudge over miles of pack ice to the exposed, rocky soil of their breeding grounds. Hundreds of pairs nest in one breeding site, with the pairs spaced just a couple of feet apart. Previously attached males take up residence in their old nests, shallow pits carved from the frosty earth and carpeted with thousands of stones smaller than a plum. Single males stake out and build nests of their own, in the hopes of one day starting a family.

When the females return, they choose mates from among the males on the nests, rejoining their companions from the previous year when possible. About half of the females hook up with new partners.

The risk of a warm spell is what motivates the penguins’ quest for stones. Meltwater from the surrounding ice can inundate the colony and cause a breeding disaster. “Everything gets thick with mud and guano and it’s horrendous,” says Fiona Hunter, a zoologist at the University of Cambridge in England. “The eggs can end up sitting in a pool of water, and they probably wouldn’t hatch because of the cold and because there’s an air exchange through the shell”—immersion might cause the embryo to suffocate.

A large pile of stones lifts the eggs off the ground and out of harm’s way. So males and females take turns scouring the area for unattended stones, often trying to swipe them from neighbors. The victims chase brazen robbers away by pecking them and bashing them with powerful flippers.

Given nest owners’ violent reactions to birds that try to steal their stones, Hunter was surprised and amused when she saw a female waddle off with a stone from an unattached male’s nest—while he looked on calmly. The female had just mated with him.

“I thought, “She’s trying to do something tricky here,’” says Hunter, who had been keeping track of which penguins were paired together. She and colleague Lloyd Davis of the University of Otago in New Zealand had previously found that one out of ten females have sexual encounters with males other than their mates, but they had never seen anything like this. The researchers kept their eyes open for more cases of penguin prostitution, and they observed a total of ten over three breeding seasons.

In each case, a female penguin left her mate and made her way to a single male at his nest. She stood nearby and gazed at him. When he flirted with her in the penguin way, giving her a sidelong glance and bowing his head, she followed suit. The hopeful male then stepped off his platform of stones, allowing her to waddle on. Leaving no uncertainty about what she was there for, she lay face down on the nest, and the male mounted and mated with her. Afterward, she got up, picked up a stone with her beak, and without further ado, went back to her own nest. In half of the cases, the female returned to the same single male for a second stone, although they did not mate again. In one instance, a female made off with a total of ten stones.

And the researchers discovered another curious behavior: Often the females took stones away from the males without offering sex in return. The females would flirt exactly as before, only they would skip the mating and take off with a stone. “It’s as if she takes the money and runs,” says Davis. Strangely, none of the males protested, though a few tried unsuccessfully to mount the females. One of the females came back for no fewer than 62 stones within the space of an hour. “These males are not very intelligent,” laughs Davis.

But perhaps they’re smarter than they seem. “The evolutionary theory behind it is that the individual’s aim in life is to pass on as many genes onto the next generation as possible, and have as many offspring survive, or survive with a good quality of life,” says Hunter.

Single males could be meeting those aims by trading stones for sex. “One argument is that by letting the females have the stones, every now and then the males get to copulate and get the chance to sire offspring,” says Davis. DNA tests on Adelies suggest the male who raises the chick is nearly always its father, so the encounters probably do not produce many offspring. But if the single male did succeed in fathering young, he would be getting off easy: He wouldn’t have to lift a flipper to raise them, and the stone he provided would literally give his progeny a leg up in the world.

Both Davis and Hunter caution that only a few cases of penguin prostitution have been documented, so it’s difficult to determine the most likely motives. But to be thorough, they list several other possible interpretations of the phenomenon.

The female could gain if her mate was infertile, and the “extra-marital affair” insured a successful breeding season. About eight percent of Adelie eggs don’t hatch--the result of infertility or a genetic mismatch between sperm and egg.

The stone could also be a justification for the female’s absence from her mate. John Reynolds, a biologist at the University of East Anglia in the United Kingdom, explains why the females might want to keep their behavior a secret: “The problem presumably is if her partner sees what’s going on, he may withhold parental care.” Hunter followed several females after their deals, and watched them return home, drop their loot in their own nests, and sit around with their mates. The males did not seem to watch the females as they left the nest and likely couldn’t see what they were doing from a distance, so it’s unlikely they were jealous. “I’m the suspicious sort, and if I were a male penguin, I would say, “Where the hell did you get that big stone?!’” Reynolds laughs.

Another possible benefit to the female is that she could be ensuring the fittest father for her chick. The sperm from each male would compete inside her to fertilize her eggs, and in theory, the “best” sperm would win. Despite the discovery in recent years that Adelies and other birds exhibit high rates of infidelity, most of the time the steady partner wins out in the end. “Whatever the mechanism of sperm competition [the long-term mates] use, it is effective,” says Davis.

Finally, Hunter believes the female may be checking out a potential future mate in case her current mate dies before the next breeding season, which happens to more than a quarter of the males. “She’s sort of started up a relationship with him,” ventures Hunter. “That’s common for seabirds that pair for long periods of time. They need to set up a partner as soon as they get to land.” After all, the birds must mate and hatch chicks in just four months, before the pack ice melts and submerges the breeding grounds.

The idea of females choosing their mates for genetic or other reasons pushes the bounds of classical theories about sexual selection. The old view held that males compete with each other to mate with a female, who has no choice in the matter. “Life isn’t as simple as it was thought,” says Reynolds. “Females have a lot more tricks of their own than anyone had ever given them credit for.”

Other animals also prostitute themselves for something valuable to them, though in most other cases, that something is food. For female purple-throated carib hummingbirds, good meals are dependent on the three key factors in real estate: location, location, location. The males of this tropical Caribbean species are larger than females and tend to monopolize neighborhoods with the most productive flowers. Females are left to settle for skimpy plots or scavenge for food. Perhaps it’s not surprising, then, that it is the females, which do not pair up with long-term partners, who seem to trade sex for the right to poach in male territories.

The negotiations have become rituals. First, the hungry female infiltrates the male’s territory and the landlord chases her out. This can happen more than five times before the male accepts the insistent intruder and allows her to feed in peace. Emboldened, the female can even nudge the male off his own perch. Then, after a brief display of aerial showmanship—hovering or flitting from side to side—by one or both birds, they mate, at times fluttering their wings to stay balanced. Finally, the female flies off, usually to get in another feeding. But the male no longer feels the need to share and chases the female off for good.

“Clearly something interesting is going on,” says Ethan Temeles, a biologist at Amherst College in Massachusetts. Researchers did not capture the females to check their reproductive states, but if, as predicted, the females were not fertile during these feeding sessions, he says the encounters would be a simple exchange of sex for food.

But in the animal kingdom, it’s the insects that turn the most tricks. The presents are so common they have a name: nuptial gifts. These range from dead prey—the insect equivalent of a box of chocolates—to food bags attached to females’ bodies during mating.

“The big question from an evolutionary perspective is, why is the male investing?” asks Darryl Gwynne, an entomologist at the University of Toronto. “There are two main theories. He could be getting direct fertilization success, or he could be indirectly contributing to the welfare of his kids.”

In the inch-long hangingflies of North America, the main benefit to the female of the gift-giving seems to be the child support payment. During the mating period, females basically stop hunting, and males go after larger prey. When a male snags something, he sends out a chemical signal, or pheromone, and females make a beeline for the meal.

As the female chows down, the male begins to mate with her. But the female is rather mercenary about the whole affair: Even though they are coupled, she somehow prevents his sperm from entering her body until she has gorged herself for a full five minutes. If, after that time, she has already devoured the insect, she will struggle to free herself from this male--he has offered her too paltry a gift. Time to move on to another one, who might provide a bigger offering.

If, however, she is still munching after five minutes, the male’s sperm will start to flow into her body. She will leave him for another male and meal if his gift takes less than 20 minutes to eat, the time it takes to fully inseminate her. But if the meal takes longer than 20 minutes, the male will struggle free and snatch back what’s left of his gift, either to eat it himself or to use it to lure another female. He is successful in that case: The female loses interest in sex for a few hours and lays eggs almost certainly fathered by him.

Randy Thornhill, a biologist at the University of New Mexico who literally wrote the book on the evolution of insect mating systems, says this behavior has evolved to provide females with the nourishment they need to produce eggs. And because a well-fed female runs less risk of getting tangled in spider webs while searching for food, he notes, “She gets the food she needs at lower cost than if she hunted it on her own.”

Her offspring benefit as well. Her eggs are enriched by the extra food and are therefore larger, which makes the offspring bigger and more resilient. “And by cutting off the copulation in five minutes,” says Thornhill, “she’s getting food but avoiding the sperm from males who might not be good hunters.”

Male decorated crickets have figured out a way to distract their potential mates long enough to inseminate them. Instead of putting sperm directly inside females, a male attaches a bag filled with sperm to the female’s abdomen. The bag takes between thirty minutes and an hour to empty into her spermatheca. Gwynne has traced the appearance of these bags of sperm back to crickets living more than 200 million years ago. And not long after the bags appeared, females evolved to reach back, remove, and eat them.

To maximize their chances of fathering young, the males also began to provide a bag of food for the females to nosh on instead of the sperm. “If females aren’t given this gift, they respond in a nasty way,” says Scott Sakaluk, an entomologist at Illinois State University. “They turn away from the male and take out the ampulla (sperm sac).”

A female given these gifts of food values quantity over quality. If there isn’t enough food to keep her occupied while the sperm is entering her body, she will reach back and start eating the bag of sperm. “A steak dinner takes much longer to eat than a Big Mac,” says Sakaluk.

But these males are not actually giving the females anything like a steak dinner—or even a Big Mac. Unlike some of their insect cousins, these males have evolved to indulge the female’s need for a food gift without actually giving her much of nutritional value. “It’s kind of a sham,” says Sakaluk. “They’re basically giving the females a big gummy bear. If you have the insect equivalent of a sweet tooth, males have a way to engage that without really having to spend too much on the quality of the gift. It’s false advertising.”

Another creature, the Australian redbacked spider, has evolved a morbid and seemingly wasteful food gift—himself. After mating with the female, the much tinier male, like a kamikaze pilot, somersaults into her open mouth to be eaten alive. His body doesn’t provide much in the way of nutrition, but biologists believe he offers it up to keep the female busy as his sperm enters her body. Now that’s quite a trick.

Maggie McKee is a science writer from Washington, DC.