You may have seen their antics on a languid summer day: Somewhere on the reedy fringes of a pond, a male dasher dragonfly pursuing a female, like two hyphens of lightning. Or a tiger-striped spiketail diving, twirling, flashing its gossamer wings, then in a blink, meeting a mate to ascend together into the ether. Or a linked pair of brilliant green darners hovering as one over the dark water, the male towing the female, darting forward, then back, then straight up with the kind of aerial agility of which we masters of the helicopter can only dream.
From a distance, dragonfly rituals of courtship and sex look harmless, even romantic. But a close look at their mating game reveals a harsher tale of sexual harassment and conflict. Take the jewelwing Calopteryx splendens. Some males dispense with courtship altogether and just snatch unwary females while they're warming in the sun—even immature ones, shimmer-fresh after emergence from their larval youth. Others, called "stealers," attack and split mating pairs by ramming, pulling, and biting them; still others, "water lurkers," grab a female in the midst of egg laying so they can have their way with her, even if she drowns in the process. Females, for their part, attempt to escape this boorish behavior by flipping, zigzagging, spiraling upward or downward, submerging in water, fleeing at high speed, or fighting back, sometimes murderously.
Why such a war between the sexes? Scientists seeking clues to the answer are finding in dragonflies a bizarre mix of cooperation and conflict, instinct and experience, which may explain not just their odd reproductive habits but also their dazzling diversity of colors and species.
When my grandmother was growing up, dragonflies were known as devil's darning needles and horse stingers, considered an annoyance by some, a danger by others. In many places the insects are still under suspicion, dubbed finger cutter, horse killer, ear stick, and eye pisser. They are poisonous. They will sew together your lips. They will crawl into your ear and penetrate your brain. They will sting you. They will bite you. They will bring you rotten luck, or worse.
"Not so," says Philip Corbet, a biologist from Cornwall in England. "Dragonflies are neither nuisance nor danger—that is, unless you're a mosquito." Or another dragonfly.
Corbet is fixed on a pair of elegant blue-tailed damselflies on the sunny bank of a small lake in Spain—one azure, one ocher, "both from the species Ischnura graellsi, renowned for having females of more than one color," he says, and also, for the male's distinctly "ungallant" behavior. "To secure a copulation, a male will seize a flying female and sometimes even bite her wings at the base."
This pair, however, is locked in an embrace that can only be described as an ersatz heart.
Anyone who has watched dragonflies mating in the bright air has seen a wonder of evolution, Corbet says. Odonates, as they're called, or "toothed ones," have been around for more than 300 million years, which has given them time to figure all the angles on sex. Judged by their longevity and diversity (6,000 species) and the scope of their distribution (every continent except Antarctica), they're one of nature's great reproductive success stories.
Corbet brings his net close to the coupled pair. He keeps the net's shadow low, then whips the net over with a quick flick of the wrist. Such skillful fliers are dragonflies and damselflies that they often make a mockery of such efforts at capture. (The difference between a damsel and dragon, in a nutshell, is that the damsel is small and slender and holds its wings over its back when at rest; the more robust dragonfly holds its wings outspread.) But Corbet is a master. As a child of six, he fell helplessly in love with the insects. Now in his 70s, with two wings of snow-white hair and a full white beard, he is the doyen of dragonflies and author of the "bible" on the subject.
He pulls the male out of the net and turns him upside down to look at his genital organs.
At the tip of the male's abdomen are its testes; at its base, behind its legs, is a penis and a small swollen pouch for storing sperm. Male dragonflies sport two sets of sex organs, the prerequisite equipment for a mating system that is unique in the insect world. Before he copulates, a male dragonfly must in essence self-inseminate, moving his sperm from the testes to the storage pouch and into the penis. Here comes the tricky part. He must grip a female by the head or thorax and hold her in the tandem position, with claspers at the tip of his abdomen that fit neatly, like a lock and key, with a special plate on her thorax or behind her eyes.
"If it seems that dragonfly biologists are inordinately preoccupied with sex, they may be excused," Corbet says. Sexual behavior is key to understanding how dragonfly species got to be the way they are. And sexual organs are key to their identity. "Slight differences in this clasperplate system are what define some species that are otherwise nearly impossible to distinguish."
Once the pair is in tandem, and the female is receptive to the overtures of her suitor, she will curl the tip of her abdomen around to bring her vagina in touch with his penis, working the pair into that heartlike copulatory position.
"It's a jolly difficult business," says Corbet, "and there's much speculation about how it evolved." Some experts believe that the male originally placed his sperm package on the ground. This was risky, given what Corbet calls the "predatory proclivity" of some female dragonflies to banquet off their partners. Males may have adopted the tandem position to protect themselves from becoming their lovers' prey. Over the ages they evolved ways of keeping their sperm packages safely tucked under their abdomens and, eventually, a complex genital "sperm bank" for storing it there.
So, too, they evolved strategies for effectively guarding their mates and fending off rivals. After sex, many pairs do not disengage but fly about in tandem, the male guarding the female by continuing to grasp her while she lays her eggs. This may serve the female, protecting her from clamoring suitors so she can oviposit in peace.
But there's nothing chivalrous about male sexual behavior. Some males embrace females with spiny claspers in a viselike grip that causes damage. Look closely at the eyes of a female darner, and you may well see dark puncture marks. This sort of abuse appears widespread among some dragonflies. In one study of 12 species of clubtails by Sidney Dunkle, a biologist then at the University of Florida, 88 to 100 percent of all females had holes in their heads, caused by a male's iron hold. The aptly named dragonhunter (Hagenius brevistylus) earned the dubious distinction of inflicting more severe damage than any other dragonfly: The spines of his appendages gouged the female's eyes, punctured and split her exoskeleton, and pierced her head, so that a "maximally damaged" female had as many as six holes of varying sizes punched in her head.
Grab, shake, bite, gouge, puncture, split, punch: It's enough to put anyone off sex.
In a brilliant experiment some years ago, Jonathan Waage of Brown University discovered the Rosetta stone to this strange mating behavior. Waage studied the jewelwing damselfly Calopteryx maculata. First he examined the sperm-storage organ of females after a couple of matings to determine whether sperm from a second mating was added to sperm from the first. He was surprised to find that the amount of sperm hadn't changed. Then he dissected pairs in the midst of copulation and studied their sex organs under an electron microscope. The experiment revealed that a male dragonfly uses his penis not just to transfer sperm to the female, but also to remove sperm left in her storage organ from previous matings. When he curls into that wheel position and begins his energetic genital thrusting, he's actually using his rigid, spoonlike, and sometimes spiky, penis to scrape out rival sperm before he deposits his own.
Such a ploy is necessary, Corbet says, because of female choice and sperm competition. A female nearly always mates with more than one male; it's in her interest to "upgrade" her fertilizations if she can, thereby exercising choice over the paternity of her offspring. Males want their sperm alone to prevail, so they have evolved strategies for purging other sperm and for discouraging mates from copulating with rivals. In this game of sexual chess, the last sperm into the female's storage organ wins by fertilizing her eggs.
Waage's discovery helps explain all sorts of cunning and perfidious dragonfly habits: why males harass females (to spread their sperm around); why they assume that weird heartlike copulatory position (the wheel facilitates the removal of rival sperm); why they guard females, and encourage them to lay eggs directly after mating.
This warring may have a surprisingly "creative" effect, says Ola Fincke, an evolutionary biologist at the University of Oklahoma. "It may be a novel mechanism for generating the different colors found among some females," she says, "and even entirely new species." In Fincke's view, the brilliant diversity of dragonflies may arise not only from adaptation to ecological niches, as with the famous Galapagos finches, but also as a response to sexual conflict.
Fincke studies Enallagma damselflies, known in North America as bluets. Mature female bluets come in two colors, the more common green type and also blue, the usual color of males. Why would females of different colors be maintained in a population? Fincke suspects that sexual harassment offers an answer. To measure harassment in bluets, she uses the "damsel-on-a-stick" technique: She glues live females to a perch and places them at the edge of a small pond, where males congregate. "Females may be harassed as often as five times a minute," she says, "and not just by their own species, but by males of closely related species." Blue females suffer significantly less.
Studies show that females constantly hounded by suitors have lower fecundity. So, in the game of evolutionary one-upmanship, females may have evolved different color forms as a response to harassment. According to one hypothesis, a blue female would be hassled less because she looks like a male. Fincke has another explanation, with some startling implications.
"It may be that a female of rarer color doesn't get harassed as much," she posits, "not because she looks like a male but because she's a less familiar form of female and doesn't fit the male's 'search image' for a mate." In recent experiments, Fincke has shown that young males discover what a female looks like by exposure. If they're reared with green females, they choose to mate with green females; if they're reared with blue ones, they'll go for blue. This suggests a revolutionary idea. Male dragonflies learn; their sexual behavior is not hardwired but more flexible, more "intelligent" than anyone ever imagined.
Like most scientists, Fincke follows questions, one leading to another. In her view, sexual conflict may explain another perplexing mystery: the relatively swift evolution of bluet species—18 new species in the past 250,000 years. Speciation is still poorly understood, and the explosion of new species in this genus in particular is a conundrum. "How do you explain the rapid evolution of dozens of different species of blue-and-black damselflies, all of them occupying essentially the same ecological niche?" she asks. Fincke suspects that females with slightly different thoracic plates are favored in evolutionary terms, because male claspers of some species won't fit with them, so not as many males can harass them by taking them in tandem. In short, sexual harassment sparks the evolution of female plates that differ from the usual, which in turn triggers shifts in the shape of male claspers, in an evolutionary tango that gives rise to whole new species and unexpected variety.
The next time a pair of elegant jewelwing damselflies or feisty scarlet darters cavort in the flecked morning sun, consider it: evolution on the wing, in motion, right before your eyes.