It's a blustery spring day in the Australian outback, the kind that makes you think rain must be on the way, although there hasn't been a drop in months, and the ground is brown and parched. In some animals, frogs for instance, a dry spring can slow down or stop altogether the normal, romantic inclinations that come this time of year. But the lack of rain hasn't deterred the male spotted bowerbirds.
Under old peppertrees, thornbushes, and stands of oleanders, they've built elaborate U-shaped arenas of dried grasses, 12 to 14 inches (30.5 to 35.6 centimeters) high and 12 to 20 inches (30.5 to 50.8 centimeters) long. They've decorated them with piles of sun-bleached sheep vertebrae, shiny aluminum foil, pop-tops from beer cans, shards of broken windshield glass, and little strips of red and blue plastic. The fanciest bowers feature special, seductive tidbits: a silver fork, the shoe token from a Monopoly game, old gun shell casings, red, blue, and purple glass of the deepest hues. The birds have arranged their treasures with an eye to the light—how does that bone pile look when the morning sun hits it?—and to their symmetry: silver metal hoops of unknown origin, for example, placed at equal distances from opposite ends of the bower.
Now a male can do little more than watch and wait. If he's built a good bower, then he'll succeed in life's ultimate contest and win the top prize: a female who chooses him as a mate.
"That's really what it comes down to," says Gerry Borgia, an evolutionary biologist who has studied the mating behaviors of bowerbirds for 23 years. "So you wonder sometimes when you see poorly built bowers," he says, pointing to one in disarray. "You want to say to the guy: 'Hey! This is about your reproductive success! Get moving! Straighten those straws! Find some more bones! Why be a C student?'"
Borgia, a hefty, middle-aged man with a broad, gap-toothed smile, bends over a video camera he's placed a short distance from the bower and changes the tape. He's stationed similar cameras with microphones at 22 bowers scattered across the sheep and cattle stations near the sleepy town of Nyngan. The cameras are equipped with motion-detection sensors and record whatever the male birds—or their female visitors—do within the bowers. Later, in his University of Maryland lab, Borgia's students will review the tapes, picking out the ones that show what male bowerbirds might dream about: a female entering the straw bower, watching the male perform and sing for her, and, if she is well pleased, accepting him as a mate. Borgia isn't sentimental about this latter event, referring to it simply as a "cop"—short for copulation.
"You watch enough of these cops, and you begin to get a feel for why the female chooses one male and not another," he explains. "It's my guess that this guy isn't going to do well. I mean, that's pathetic," he says, waving his hand at the bird's puny pile of vertebrae. "And the thing is, he took over this site from an older male who died, but who had a great bower with lots of bones. And they're still here! This new guy just hasn't made the effort to move them to his bower."
Borgia shakes his head like a teacher who can't figure out why some kid who has everything handed to him on a platter would still choose to fail. "He's probably not getting any cops this year," the professor says, assigning the bird to possible evolutionary oblivion.
As if in protest, the male, a blue-jay-size bird colored beige and brown, squawks at us from a nearby eucalyptus tree. He rasps out a long series of skraas, then changes to the snarling, spitting sound of a cornered cat, and ends with a laughing call that sounds like a kookaburra.
"He's trying to scare us," Borgia says. "They're great imitators—cats, hawks, kids crying. They use that skraa call in their courtship displays too, so there must be something about it that allows females to find genetically superior males. But he's got a lot to learn about how to build a bower, one that will attract the females and get him some action."
The most successful males are about ten years old and have spent some five lonely bachelor years perfecting their skills. In this species (as with most birds), a male can't force a female to mate. Like a solo rock star, he must devise a bower, song, and dance that wows the gals. Among bowerbirds and most other animals as well, it's the females that do the choosing.
From fruit flies to elephants, females pick the male (or males) with which they want to mate. The males, in turn, compete with each other to get a female's attention, each vying to show her that he will be the best sperm donor for her babies. That is why, evolutionary biologists say, males are most often the ornamented sex. It is why the male peacock unfurls his dazzling train, why male guppies are adorned with bright orange and blue spots, why male frogs call and male canaries sing. It is even why the genitalia of many males, particularly insects, are as fancy as an Aborigine's embellished didgeridoo, with accoutrements far beyond what's required to get the job done.
"Basically, the male wants access to the female's eggs," explains William Eberhard, an evolutionary biologist at the University of Costa Rica. "And he'll do whatever it takes to please her. But it's her game; she sets the rules. And she makes the choice."
Charles Darwin was the first scientist to devise a theory of sexual selection and to recognize that females frequently select mates. He began to develop the notion while writing On the Origin of Species, in which he argued that the related theory of natural selection is the primary force in the evolution of all organisms.
Natural selection goes far in explaining why one individual animal survives to pass on its genes to the next generation, while another dies leaving no descendants. It is why female birds are often drably colored (to hide from predators when incubating their eggs), and why gazelles are built for speed (to outrun their enemies). But natural selection does not explain features that would seem to hinder an animal's survival, such as the male peacock's extravagant plumage or a male elk's heavy and unwieldy antlers. How did such unlikely traits—ones that seem to run counter to every Darwinian rule for staying alive—come about? Even Darwin struggled to find a reason, once writing to a friend, "The sight of a feather in a peacock's tail makes me sick!"
Eventually Darwin devised a solution, explaining in his 1871 book, The Descent of Man and Selection in Relation to Sex, that males' bright colors, baroque ornaments, and elaborate songs are the result of a process he named sexual selection. According to Darwin, sexual selection shapes species in two ways—by giving rise to competition among males for mates, and via females' decisions to mate with particular males.
Darwin's fellow evolutionists readily accepted the part of the sexual selection theory suggesting that male competition plays a role in evolution. Many males are equipped with horns and antlers or other weapons, while females are not, and it's easy to see that a male elk with a large rack would have an advantage over his rivals. He could use his antlers to defeat his competitors and mate with more females. And that would give him the chance to have more sons that would inherit his genes for big antlers and his abilities both to defeat other males and inseminate many females.
But the part of the theory suggesting that females choose mates—thus shaping male physiology and behavior and influencing a species' evolution—was immediately attacked from all sides. Another proponent of the theory of evolution, Alfred Russel Wallace, particularly despised the notion and actively lobbied against it. He argued that males were brightly colored and given to song because of their "superabundant energy" during the mating season. For Wallace, natural selection covered everything, including male competition. And he found the idea that females choose mates because they prefer a particular color or ornament ludicrous because it suggested a faculty for taste and discrimination that he believed to be beyond most animals. Throughout most of the 20th century Wallace's opinion prevailed, and Darwin's theory of sexual selection, with its offshoot of female choice, was largely ignored.
"Right into the 1970s people were still laughing at the idea of female choice," says Michael Ryan, an evolutionary biologist at the University of Texas in Austin. "One writer even said that all you had to do was look at our own species to see that females had no input whatsoever in mating decisions. Now, of course, we have tons of examples that show that Darwin was right: It's most often the females that choose."
Indeed, these days scientific journals are packed with papers on sexual selection and mate choice. In their search to understand how and what females choose, scientists have uncovered an entirely new world of the startling and steamy: Fruit flies that (for their tiny body size) produce some of the largest sperm in the animal kingdom; male millipedes with special legs that exist solely to rhythmically massage a female's reproductive tract, apparently a stimulation she needs before allowing him to inseminate her; a protein in a male mouse's saliva that tells a female mouse if he's Mr. Right.
And they've discovered that the females of numerous invertebrates are equipped with sperm storage organs, special pockets where they hold the male's fluid, perhaps assessing its quality. Scientists speculate that the females may nurture the sperm if they accept the contribution, or destroy them if not.
The biggest boost to the theory of female choice came from a highly influential paper written by evolutionist Robert Trivers in 1972. Reproduction is not an equal equation, said Trivers. Males and females invest different amounts of energy and resources into producing offspring. Males produce many relatively cheap sperm, but females make a set number of expensive eggs. So it makes sense that males compete for access to females, and that females are choosy about the male, or males, they let fertilize them.
The big question then becomes: What do the females want?
Some researchers have speculated that a male's ornaments and vocal beguilements carry information about the quality of his genes, or his immune system, or his parenting abilities. Others have suggested that there is little information in these secondary sexual traits; they exist solely to attract the female. If she chooses a mate that other females regard as handsome, she'll produce attractive, sexy sons who are more likely themselves to be chosen as mates, and so pass on her genes.
Michael Ryan contends that although the male's trait itself—the color he displays or the sound he makes—may be arbitrary, there's definitely a reason for the female's choice. "It's generally something that the male has hit on that stimulates something in the female's neurons," says Ryan, who has subjected a variety of species to mate-choice experiments devised to get a female to tell all.
Ryan leads the way into a lab where a walnut-size female Tungara frog swollen with eggs is about to take such a test. In the wilds of the Tungara frog's native Panama, Ryan explains, the males gather in small pools to belt out two-part calls: one part a deep chuck sound and the other a higher pitched whine. The females hear potential consorts and swim to the ones they choose. A selected male climbs aboard a female's back, and she carries him off to fertilize the eggs she will eject.
"The whine portion of the call identifies the species," says Ryan, in essence telling the female, "I'm a male Physalaemus pustulosus." And the chuck indicates the male's size. "Bigger males make deeper chucks," he says. "Females prefer the males with the deepest chucks." Deepest chuck, biggest male, most sperm: By choosing him, a female has the best chance that all of her eggs will be fertilized.
But that's not the end of the story. A lone male with no competition may not make the chuck call; he may only make the whine and still get a female. Not until other males show up does he add his deep-throated love tone. The reason is that the love song has a mixed blessing: Female frogs aren't the only ones listening for big males. Bats, opossums, and other predators are too.
"It's a good example of the dilemma males can face," Ryan says. "If a male has to compete with other males to get a female, he must make the chuck call. But the call puts him at risk of being eaten, and thereby removed from the gene pool altogether."
Despite the dilemma of the love song, it's clear what a female Tungara frog is looking for: the biggest male, who can fertilize the most eggs. But sometimes scientists are less sure of what a male characteristic might be saying to a female. Ryan and graduate student Molly Cummings have studied a Mexican swordtail fish, Xiphophorus multilineatus, and found that females prefer males with shiny tails.
"We haven't figured out what that shine tells the female about the male," says Cummings, "but females seem to like the brightest males."
One thing the shine does do is sidestep the predator problem faced by male Tungara frogs. "This is what you and I see," Cummings explains, setting a photograph of a gray-black fish on a table. "And this is pretty close to what a female X. multilineatus sees," she says, setting a second photograph, taken under UV light, next to the first. The tail shines with silvery discs and streaks.
It turns out that swordtails can see in the UV light range, but, like us, their predators cannot. So the male swordtails seem to have evolved a less risky way of saying to their females: "Look at me. I'm the best."
In other cases, researchers have a clearer idea of what male coloring tells a female. In a species of guppies named Poeecilia reticulate, successful males generally have richly colored red-orange spots and stripes along their sides, says Greg Grether, an evolutionary biologist at the University of California, Los Angeles. "They can't make that color without eating a particular orange fruit that's desirable but fairly rare in their native streams in Trinidad," he explains. "So the orange may indicate which males are best at finding the fruit or at outcompeting other males to get to it first."
Scientists have even succeeded in deciphering the message a female reads in a male peacock's train. In a study that surely would have cured Darwin of his loathing for peacock feathers, biologist Marion Petrie showed that the best dads were indeed the fanciest ones. Their chicks weighed more at birth than did the others, and those same chicks were better at evading predators.
Darwin postulated that female choice not only could change the characteristics of a given species, but also lead to the creation of new species entirely. Studies of such species as the giant-sperm fruit fly, Drosophila mojavensis, may explain how this can happen.
In her University of Arizona laboratory in Tucson, Therese Markow uncorks a glass vial containing dozens of male fruit flies living on a bit of lab culture. She drops in a short rubber aspirator, takes aim, sucks up a few flies, and transfers them to another vial containing females.
For a few seconds the males simply sit and preen. Then one of the males moves toward a female and pulls his wing to one side, producing a soft buzzing sound.
"OK, he's starting his mating song," says Markow. "If she likes him, she'll sing back."
Like voyeurs, we watch the couple in the glass vial intently.
"Well, she doesn't like him," Markow laughs. "She's not singing back."
The male persists, now vigorously scissoring both wings; the female remains unimpressed. "Now she's singing her 'I don't want you' song," says Markow. "That poor little male; he's just singing his heart out for her."
Behind them, closer to the end of the vial, another female does scissor her wings in acceptance, and the male mounts her.
"These flies are from the same D. mojavensis population so that's what I would expect to see: Even though one female says no, another says yes pretty quickly," says Markow.
But when the males and females come from D. mojavensis populations that are geographically separate, the females of one group rarely accept the males of the other group, even though they are members of the same species. In the wild, D. mojavensis lives in rotting cactuses in both mainland Mexico and Baja California, separated by the Gulf of California. "The two groups can mate and produce viable offspring" says Markow. "But the females prefer not to. So I think what we're seeing is a new species in the making." The initial separation may have been triggered by the Gulf of California, a natural barrier that keeps the two populations apart, "but female choice maintains and reinforces that division," Markow explains.
Such simple preferences on the part of females—for a male of a certain color or shape, or from a particular population—are now thought to be the primary cause for the diversity of wildly decorated jumping spiders found in the Sky Island mountains near Tucson, Arizona, and for the even greater variety of cichlid fishes in Africa's Lake Malawi.
"There's no question that Darwin was right about the power of female choice," says Markow. "It can shape males and it can make new species."
And what is it like to be the waiting male, to be Mr. Lonely Heart? To find out, I set up a blind close to the bower of one of Borgia's spotted bowerbirds, a male the scientist says was the "big scorer" the previous year. Borgia has named each bird for the location of its bower. This top bird has built its mating arena in the shade of two old peppertrees on the Gerar Station, and so is dubbed "Gerar Pepper Bower." I nickname him "G.P."
Unlike the bower of the C student, G.P.'s is a sturdy, handsome structure, its decorations artfully arranged, its straw walls thick and symmetrical. In the center he has piled shattered bits of windshield glass, each piece about a half inch (1.27 centimeters) in diameter. When the sun hits them, they glitter like diamonds. He's hung some bits of metal wire and a strip of red plastic along the bower's walls and stacked a long, thick wall of sheep vertebrae just beyond one end. At the opposite end lies an equally large pile of clear and colored glass, sprinkled with a few shell casings and aluminum pop-tops. Other smaller piles of glass and odd pieces of aluminum foil and plastic lie scattered in a mosaic pattern around the bower, some as far away as four feet (1.2 meters).
"Oh yes, all that is part of his display," Borgia says, when I ask about some seemingly random bits of glass. "Everything here that's not natural is part of his bower."
A male can build a straw bower in the space of a few days. Decorating it, however, takes several additional days, and getting the ornaments in the right place can take years. Spotted bowerbirds build their bowers anew each year, usually locating them close to those of the preceding mating season. And when an older bird dies, a younger one—perhaps a son or other close male relative—takes over his locality and his treasures.
"All these decorations, what the males choose and how they place them, is driven by female choice," Borgia says. "In a small way, they're like us: The male's ornaments aren't necessarily a physical part of him, but are more in the things he acquires."
Indeed, the male and female birds look very much alike—brownish and speckled with golden dots, a spray of bubble-gum-pink feathers on the back of their necks. These are usually hidden from view, but males and females unfurl them in times of aggression, and the male also fans them out when courting a female or when practicing his mating show.
I saw many such practice runs over the next four days. Sometimes G.P. perched on a branch beside his bower and rehearsed his screechy love songs, which resembled the harsh blast of steam from a cappuccino machine. Sometimes he walked the short length of his straw bower, licking every individual straw to leave behind traces of his saliva. Or he would rearrange a pop-top here, a plastic ring there, or drop one of his shell casings on the pile of glass, then cock his head to listen to the pretty ching it made. I imagined he would like to make that sound for a female.
Sometimes one or two other males arrived to check out the competition or to try to steal one of G.P.'s objets d'art. But he was vigorous in defense of his bower and belongings, and flew at them with beak and tongue out, claws ready to strike.
One afternoon, after another long, lonely day, G.P. picked up a bunch of green pepper berries, fluffed up his pink topnotch, and raced around and through his bower, screeching and clucking and looking rather ridiculous, like any poor soul waiting for the phone to ring. Alas, I was the only female in view.
Or maybe not. Perhaps another one—one of his own species—was watching from the safety of a nearby eucalyptus. Young females may make multiple visits to several bowers, studying them and the males, learning, Borgia thinks, how to choose. They get nothing from the male beyond his genes; he does not help to raise the chicks. Nor do females appear to mate with more than one male in one season. "She studies them and makes a choice," says Borgia, "and if she's happy, she'll return to the same male the next year."
Were none of the females watching G.P. pleased enough? Or was it merely a slow period in the season? The wind blew steadily most afternoons, and G.P. often flew away when it started to kick up, apparently deciding it wasn't worth his time to wait.
And then, on the fourth morning, a female appeared. She perched on the branch beside the bower for a minute, then hopped right inside. G.P. went berserk, squawking and fluffing and racing around his bower. He stopped at one end and picked up a pop-top to show her, then dropped it and did another lap around the bower. She just watched. Then she began to lower herself, ever so slightly lifting her tail, tipping her head forward. Borgia had told me that was the "choice" sign, and I held my breath.
G.P. screeched even louder and hopped toward her. And at that very instant, another male appeared. Romance gave way to a brawl, and the female flew away.
But I was sure she had made her choice. She would be back, and G.P. would get another chance to keep his genes at play in the game of life.