Darwin's Island (32 page)

The interaction between plants and pollinators is a matter of economics - and economists have been quick to notice. Signalling theory tries to explain how decisions are made when the information available is less than perfect - what used car to buy, who to hire for a job, what flower to visit. One test is to look for a reliable sign of quality, whatever it might be. An applicant for a job in a bank might have a first-class degree in genetics. Useless as that certificate might be to a prospective financier, it is at least an honest (and expensive) statement of overall merit. The system works well - as long as everyone is honourable. Sometimes they are not. Straight fraud - a forged Harvard degree - can often be picked up but what of a parchment from one of the many bogus universities that nowadays advertise their wares? The University of Dublin sounds respectable but is a website. How can employers tell Redding University (an American degree mill) from the University of Reading (a respectable institution to the west of London)? Thousands of people now have such qualifications and if too many degrees turn out to be false then the whole machine breaks down. The risk is real. Nine-tenths of the ‘Tiffany’ jewellery on sale on eBay is fake, and Tiffany & Co. has spent millions in attempts to shut down the sellers, who cause huge damage to its brand. If the bogus continue to prosper at the expense of the genuine, the entire jewellery market may collapse.

A study of the economic implications of such false signals (or ‘asymmetric information’, as financial experts call it) won the Nobel Prize for Economics in 2001. Plants and animals have done such sums for years. Most of the time, they get it right and honesty more or less prevails. Sometimes, the cheats get in, for if the reward is large enough and the penalty for swindling not too stringent, natural selection can favour sharp practice. The temptation to invest in display rather than product means that the price of sex is eternal vigilance. Some orchids - like some traders - allow others to pay for the publicity while they double-cross their pollinators. Life at the top faces a constant challenge from fraudsters.

Plenty of pollinators, too, are duplicitous. Insects gnaw into a flower to gain a reward at minimal cost while humming birds can poke a hole in its side to do the same. Even legitimate pollinators like honey bees become robbers at once when someone else has broken in. For them, dishonesty pays and they turn to it whenever they get a chance.

The flowers have hit back. What they offer may be quite different from what they promise. Orchids have a wide range of lures. Some subvert their pollinators’ desires with blossoms that resemble female insects. The flowers are larger than real females, and may emit a hundred times more of their attractive sexual scent. The male bees or spiders - understandably - try to copulate with their spurious brides and in their failed attempt to pass on their own DNA do the same job for the plant. Their amatory experience is futile but intense, as many of the befuddled males produce copious amounts of sperm that costs them a lot to make and goes nowhere.

Darwin found it hard to believe that a bee could be so stupid as to frot a flower but, in the world of sex, stupidity can pay. A naive male bee faced with females in short supply, as they often are because males emerge earlier in the season than their partners, is well advised to travel hopefully because he might arrive; he should copulate with anything that looks even a little like a member of the opposite sex on the off-chance that, now and again, he will be lucky. The bees oblige and, most of the time, the orchids win. Other orchids exploit the aggressive, rather than the amatory, instincts of their pollinators. They mimic a male insect rather than a female - which annoys the local territory-holder who tries to drive out the supposed intruder and pollinates as he does so.

Other kinds exploit the greed, rather than the lust, of their visitors. They advertise not sex but a free meal but again, they provide nothing. That baffled Charles Darwin. It was ‘utterly incredible’ that ‘bees . . . should persevere in visiting flower after flower . . . in the hope of obtaining nectar which is never present’. He suggested instead that the empty flowers had hidden reserves, which the insects would reach if they made a hole and sucked the plant’s juices.

Life is less honest than he imagined and the flowers were in fact cheats. About a third of all orchids act in this underhand way - flashy signal, but no food reward. Some other plants do the same, often with a few ‘cheater flowers’ on an individual in which most are honest, but the orchids are the real confidence tricksters, for they make up nine-tenths of all flowers known to fool their visitors. DNA shows that the habit has arisen again and again within the group - but it does not always pay, for some orchids that now provide a generous recompense to their visitors have evolved from species that once led a dishonest life.

Often, such false flowers are - like the harmless flies that look like wasps - mimics, with a resemblance, more or less accurate, to other local plants that do make a reward. They flaunt a badge of quality such as bright colour to attract an assistant on the cheap. Some work hard to fool their visitors and are uncannily similar to a particular model in shape and colour. Certain Australian kinds, for example, look like mushrooms and are pollinated by fungus gnats in search of a place to lay eggs. A few even make small orange and black spots on their flowers which attract aphid-feeding flies that see the spots as potential prey. More often, their displays are no more than general statements of reward that attract a variety of insects. The parasite joins a whole guild of locals in which the various species share a resemblance and attract about the same mix of insects. Honest plants pay the price when insects avoid them after an anticlimactic experience with a cheat. Some orchids are doubly duplicitous for individuals vary in colour, one from another, which allows them to parasitise a wider range of victims.

The cheats tend to grow scattered among their hosts, for a group of fraudsters close together is soon detected by the pollinators, who move away to a more worthwhile patch. They do best at fooling insects that have just emerged into the wicked world and have not yet learned to detect double-crossers. As a result such orchids tend to flower in the spring rather than later in the year. but in many cases a shortage of pollinators foolish enough to revisit a dishonest plant force it to make a long-lasting flower and pollen that, unlike that of most of its fellows, survives for weeks or months. A certain Australian orchid uses the opposite strategy, for all the plants open on the same day of the year, giving the pollinators no time to learn about the gigantic fraud being perpetrated upon them.

Experienced insects soon become cynical for they move away faster - and fly further - from empty flowers than from those with nectar. The dishonest orchids may reap a subtle benefit from their disappointed visitors, for the still hungry insect may buzz off to a new individual, rather than shifting its attentions to a second flower on the same plant. Such behaviour cuts down the chance of self-fertilisation.

Orchids may be the real experts, but plenty of other associations between plants and pollinators have been subverted by natural selection. Wild peas and beans often make nutrient-rich rewards that attract birds to spread their seeds but some of their offerings contain nothing of value although they look like a tasty meal. Yuccas - those spectacular flower spikes of the American deserts - are pollinated by a certain moth, who carries a bundle of pollen to the female, inserts it in the right place and then lays her eggs within the flower. When they hatch, the larvae feed on the seeds and once adult fly off to pollinate another yucca. Close relatives of such moths, though, eat the seeds without bringing pollen.

 

The fraudulent orchids and their fellows among the pollinators were an introduction to a wider world of sexual dishonesty that has emerged since Darwin’s day. When it comes to the need to pass on DNA on the cheap, animals are just as devious as are plants (although not many can match the orchids, in which an entire species may transmit its genes by Machiavellian means). Plenty of animals are bullies who boast of powers that they do not possess, or swaggarts who claim sexual prowess but in truth are feeble. An ability to roar even when filled with parasites or a readiness to die in the battle for a mate is hard to fake but, as in the orchids, a dependable statement of quality can sometimes be subverted.

Many male insects use a gift of food to persuade a female to copulate with them. Dance flies, hairy-legged predatory insects of wet places, make swarms in the mating season. In some species, each male brings a gift of a dead insect larva, and mates with his female while her attention is diverted by the meal. Once the bribe has been eaten, the male is pushed off. Other species prolong the sexual experience, for they wrap the gift in a silk purse, which the female must open before she can eat. At once, a chance to cheat presents itself - and it has been seized. Some male flies make elegant and complex purses that take a long time to open, but - like a dishonest orchid - are empty, or contain a desiccated corpse. By the time the female finds out, she has been inseminated. Fireflies are just as devious. Males bring a gift, a sticky mass of nutritious gel that goes with the sperm and is soaked up by their mates. Those who can afford more of the stuff make a longer flash and attract more females. A successful male soon runs out of energy. Some cheat, with a long flash and no reward - but they take a risk, for a certain predatory firefly uses the burst of light to find its prey. A false flasher risks death every time he exposes himself.

Darwin’s perplexity about the dishonesty of orchids opened the door to a whole universe of evolutionary discord. Many creatures are happy to lie in the race to pass on genes. The conflict extends beyond plants and pollinators, to predators and prey, pathogen and host or men and their domestic animals, all of which are locked into an endless - and often joyless - conflict. Such ancient disputes explain why the Irish had a potato famine, why some diseases are virulent and others not and why the Argentinian Lake Duck has a corkscrew-shaped penis longer than its own body.

Sexual dishonesty is widespread. Birds are at it all the time. Many species appear to live as faithful pairs, but paternity tests show that the majority are happy to cheat and that half - or even more - of the eggs of a particular female are the scions of another male, often an individual more dominant than their regular partner. Mammals are even more devious. The joys of paternity-testing reveal that a male mammal’s sexual displays are often subverted: a feeble individual can sneak in when the top stag is preoccupied with display and insert his own genes with no need for a huge investment.

Monogamy is rare, for not more than one mammal species in about twenty (some humans included) appears to indulge in it. Even some classic examples of reproductive honesty are in fact cheats. The prairie vole seems to stick to his mate through thick and thin and helps raise the young. Their happy marriage is based on a certain hormone. On his wedding night a surge of the stuff kicks in and appears to tie the male to his partner for life. A director of the US government’s family planning program saw the vole as proof that sex before marriage disrupts brain chemistry and leads to divorce. The hormone, he says, is ‘God’s superglue’. It bonds partners together and, said the politician, it does the same for society (and also proves that abstinence is the finest form of contraception). The gene that picks up the hormone in the bloodstream comes in several forms in humans, too, and - in Sweden at least - men who bear two copies of a certain variant are less likely to be married or, if they are, have a more difficult relationship than do others.

The cold eye of the paternity-tester has now fallen upon the private life of the prairies. DNA cannot tell a lie - and it shows that beneath the vole’s upright social habits lies a dark sexual universe. One in five of the young of each pair is fathered by a male other than the marital partner and around a quarter of all males and females have sex outside the household. Voles are socially faithful, but sexually fickle; happy to cheat, but quick to forgive. Foxes are even more dishonest, for more than three-quarters of their cubs are fathered by a stranger.

 

Darwin was surprised by the reproductive fraud he found among orchids - but refused to accept that the same could be true for mammals, for humans least of all. In his view of sexual selection, males might be promiscuous or even crafty, but females were monogamous; they chose, and males competed for their attentions. Part of that Puritan philosophy was due, perhaps, to the social climate of the time and his reluctance to shock the female members of his household. In modern society, in contrast, the concept of dishonesty in sexual relations has almost disappeared as most liaisons consist of longer or shorter periods of serial monogamy, accepted by both parties. That shift shows the flexibility of human behaviour and how hard it can be to draw any worthwhile lessons about our own private lives from those of other mammals, let alone of flowers.

Even so, there has been plenty of reproductive dishonesty in our own history. Casanova, himself of uncertain paternity, posed as a soldier, a doctor, a diplomat, a nobleman and a sorcerer to gain the favours of an admitted hundred and twenty women (plus, more than likely, many more). He was a great lover, and a better liar, even if, according to a contemporary, he ‘would be a good-looking man if he were not ugly’. His wit, rather than his looks, charmed his way into the bedroom.

Now, the chance for deceit has been much improved by technology. No longer does a hopeful male need to display his talents directly; instead he can say what he chooses about his looks, his education and his wealth on an online-dating site. There he has no fear of detection, at least until his first appointment with a prospective mate. Tens of millions of people use such sexual aids, and millions of liaisons (many ending in marriage) have emerged from a digital romance. Even so, nine out of every ten users - and women more than men - are convinced that the world of electronic eroticism is filled with cheats, with dirty and decrepit Casanovas who present themselves as young lovers in the hope of reproductive success on the cheap.