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SEX is a risky business in the animal kingdom, especially for the guys. Take the dangerous love life of the South American knife fish. Males attract a mate by emitting electric signals over a wide range of frequencies. Unfortunately for them, their low “notes” are such an effective beacon to predators, including electric eels, that by the end of the mating season there are almost no male knife fish left.

But what else is a fella to do, when females seem to go for the gaudiest, loudest males? American song sparrows, for example, are hard to miss when courting. The male sings loudly from a branch out in the open, easily seen and heard by hungry hawks as well as female sparrows. And it’s the same for countless other species. If the coded flashes of a male firefly are spotted by a female of a different species, the hapless Romeo is likely to end up as dinner rather than a mate. In Panama, predatory bats home in on the night-time love calls of male tungara frogs. And a male cricket’s song can earn him a mate—or attract a parasitoid fly that lays its eggs on the suitor, sealing his doom.

Why do males have to put on such a show when it puts them at obvious risk? The question has been hotly debated by the finest minds in biology from Darwin onwards. Perhaps showy males are proving that they are fitter and healthier than drab ones, which is currently the most popular hypothesis. Or it may be outlandish female tastes that are driving prospective mates to evolve flamboyant sexual displays—the theory of runaway sexual selection. But neither of these theories tells the whole story because it turns out that females aren’t always attracted to risk-takers, and on closer scrutiny, even high-profile males can be more cautious than it might appear.

Even the seemingly suicidal knife fish hedges his bets. Philip Stoddard of Florida International University in Miami has found that male knife fish emit high-frequency electric signals throughout the day, but only crank up their low-frequency output during the evening, when females spawn. “If they don’t use low frequencies, they’re not gonna get the babes,” says Stoddard. But by emitting the full range of signals only in the evening, they minimise the risk of being eaten and maximise the chances of passing on their genes to the next generation.

Sexual balancing act

And many other animals are even more subtle. Lacewings serenade their mates by vibrating the plants they rest on, rather than producing a song that could be heard by predators. The feathers of the male Guianan cock-of-the-rock, which are brilliant orange in sunshine, fade into invisibility in forest shade, where it lurks when not showing off to females. And when hungry bats are on the prowl, male tree frogs utter shorter calls or sing near loud waterfalls that mask the sound.

Even more surprisingly, it turns out that under certain circumstances females may actually find discreet males more sexy than showy ones. This is the case for the Trinidadian guppy, a tiny fish that has taught scientists more about the sexual balancing act than any other animal. “Guppies specialise in blue, red and ultraviolet—colours that their predators can’t see,” says John Endler of the University of California at Santa Barbara. They court early in the morning and late in the afternoon, when their predators are least active, and when the low light shows up their colour spots to best effect for appreciative females. But Endler has also shown that where predators are common, male guppies have evolved drab colours compared to the bright spots they flaunt where predators are few.

One explanation is simply that brightly coloured males are more likely to be eaten, leaving the dull ones to reproduce. But drab males may prevail under these circumstances because females like them that way. Laboratory experiments show that females are more likely to mate with a drab male if they know a predator is nearby.

Danger may force them to be less picky. “If a female chooses a mate at random it’s quicker—she spends less time around conspicuous males, whose proximity can make her more vulnerable to predation,” says Endler. Alternatively, female guppies may find dull colours more appealing when the threat from predators looms large.

Either mechanism could explain the patterns of guppy evolution Endler has seen in the lab and in the wild. Whichever it is, a female’s change in preference is likely to be innate rather than learned. “Learning is slow and might be dangerous,” says Endler, “so a genetically programmed reaction to predators would have higher fitness and is likely to spread through the population.”

This isn’t the only instance of females changing their preferences depending on the situation. Crickets do it too. Males produce their mating trills by rubbing two wing parts together, like a bow against a violin string. They do this from the relative safety of a crack in the ground. All things being equal, females will always choose males with long trills over ones with short trills, but Ann Hedrick of the University of California at Davis has found that females factor in the risks of predation when picking a mate.

Hedrick played recordings of long or short trills in an experimental mating arena that contained both cover and open space. Then she waited to see which call drew the female. The outcome depended on where the call was coming from. “I offered females a choice between a short call with cover in front of it versus a long call in the open,” says Hedrick. “When you put them in that conflict situation, where they hear the call that they like but it feels unsafe to go that way, many of the females instead go towards the short call through cover.” With no cover on offer, the same females throw caution to the wind and always choose the long call.

It’s not clear why female crickets are attracted to long trills. They may be an indicator of quality—an example of the “handicap principle” whereby sexual signals must cost the animal something to prove their worth. “We know that trilling takes a lot of energy,” says Hedrick. Alternatively, males could have been forced to evolve ever-longer trills simply because females like them. This process of runaway sexual selection results in a trait becoming more and more exaggerated until its cost to a male’s survival outweighs the benefits of attraction. Evidence that male crickets take it to the limit comes from Hedrick’s discovery that those with the longest trills are also the most cautious—hunkering down and hiding in their cracks for longer when predators are about. “There’s more than one way of being an effective male cricket,” concludes Hedrick.

Another way to mate effectively without drawing attention to yourself is to exploit the bold display of a less careful guy. Male wax moths have been known to hang about silently near a singing rival, then waylay females who come in search of the vocalist. Some male crickets also loiter near competitors and seem to be using the same strategy.

Sneaky ploys are found among the males of many other species, including guppies. Here, the cheats bypass the whole courtship ritual, which entails quivering in front of a prospective mate to show off your colours. They choose instead to force themselves on unresponsive females. The strategy is more common when the risk of predation is high, when females tend to lose interest in sex.

In this case there’s no indication that females actually find the cheats attractive. But bluegill sunfish may. Here males come in two kinds: big guys who defend territories and display to females, and little guys who look similar to females. The smaller males don’t court females directly. Instead, they wait near a big male’s territory, and when a female swims in to lay her eggs, the little guy darts in and releases some sperm.

Many biologists see the bluegill sunfish as a classic example of a sneaky mating strategy, but not Amotz Zahavi of Tel-Aviv University. He’s the originator of the handicap principle theory, and believes there’s no sneaking going on here, just honest signalling of intention on the part of all three players. He argues that females prefer territories where their eggs will be fertilised by both kinds of males—so a big male should welcome a small male, because the two of them together will get more mates than either would alone.

Zahavi argues that any communication—sexual or otherwise—must be associated with some cost, or handicap, to prove its honesty. “Where two individuals collaborate, the signal must be loaded with a handicap, there is no other way,” he says. Zahavi acknowledges that when the cost of a signal becomes too high, it will disappear—or become covert, like the love-vibrations of the lacewing. But he believes that nature demands honesty in courtship, and that behaviour now seen by many biologists as “cheating” will ultimately be explained in terms of straightforward signalling.

The handicap principle is the most popular explanation around for the evolution of showy males, but the discovery that it isn’t the only way to woo has left some biologists questioning a theory that puts honesty at its core. “Zahavi thinks the handicap principle is everything,” says Endler. “His argument isn’t wrong, it’s just incomplete.” Endler argues that any kind of mating strategy can evolve provided it works—that is, it will increase an individual’s chances of producing offspring that will adopt the same strategy.

Is honesty irrelevant? Is it anthropomorphic to describe evolution in terms of honesty? Can a single principle really explain the bemusing array of sexual behaviour found in the animal world? The debate will continue, as surely as fireflies glow on June evenings. But it’s worth remembering, the next time you see those ethereal glimmers across a summer meadow, that there’s more to courtship than meets the eye.