Darwin's Island

by Steve Jones

  When the pollinator enters, some means is found to attach male sex cells to it. Many orchids have a spring-loaded mechanism that fires a mass of pollen in the right direction. It sticks on with powerful glue. As Darwin found by stimulating the flowers with a pencil, the stalk of the transferred pollen sac quickly dries out and the mass of male cells takes on a more vertical position, just right to fertilise the female part of the next plant visited. In a few kinds, should the mass miss its target, its energy is enough to shoot it for a metre away from the plant (the pollen is ‘shot like an arrow which is not barbed’). The blow is unpleasant enough to cause an insect that has been hit to concentrate, if it can, on the female part of the flowers it visits subsequently, which is a real help to the male who scared it off. In other species, the pollen masses crack open to the sound of a buzz like that of a particular species of bee. Yet other kinds have a see-saw that tips the insect on to the crucial male cells. It pays the plant to do the job as well as it can, for many orchids are limited in their ability to reproduce by a shortage of visitors.

  Once the pollinator has been enticed to arrive it expects to be repaid. The first reward of all, in the earliest flowers, was pollen itself, which is expensive as it contains lots of protein. Even so, plenty of orchids still provide a solid meal made up of the stuff, or of bits of tissue that resemble it. Others give nectar, which is simpler and can be provided in very dilute form. Honey bees, for example, must extract the sugary liquid from several million flowers, a few of which may be orchids, to make a kilo of honey.

  Some botanical entanglements are intimate indeed. Certain bees are so tied to their partners that their own sex lives have come to depend upon them. They obtain their sexual scents - their pheromones - from an orchid flower and without a visit they are unable to mate. The pheromones may have more than a dozen ingredients. As in the Chanel factory, the bees practise ‘enfleurage’: they mix an odoriferous base taken from the plant with an oily substance of their own that helps the smell to persist. A special grease is smeared on to the flower and the sexual mix transmitted to pockets in the bees’ hind legs. The habit evolved from the insects’ ancient habit of marking their sexual readiness - like dogs around lampposts - with scents extracted from flowers, rotten wood and even from faeces.

  The battle is not evenly matched, for the insects themselves - many of whom visit a variety of plants - are under less pressure to retain an accurate fit with their partner than are the flowers. The orchids evolved well after insect pollination began and have had to adapt to the needs of their partners, rather than the other way around. Some insects - many bees included - are quite catholic in their tastes and some orchids are indifferent as to who moves their pollen, as long as somebody does. A few species are visited by more than a hundred different insects, while only around half of all orchids are more or less faithful to a single pollinator. To become too closely connected to a particular insect is risky. Darwin himself speculated that the giant orchid of Madagascar would disappear if its specialised pollinator died out, and he may have been right.

  The orchids face a higher risk of failure if they cannot find a pollinator than do animals in the same predicament, for an insect can always try another kind of flower if its prime source of food becomes too rare or too mean. Many flowers - those of orchids included - are in fact visited by several pollinators, even if particular species do tend to concentrate on similar insects; on long-tongued bee-flies and long-tongued flies, or on tiny bees, flies and beetles, each of which picks up the pollen on its legs. Even the bees that pick up their own sexual scents from an orchid are less dependent than they seem. A certain South American species has become naturalised in Florida, where its host does not grow. It finds its chemicals instead in aromatic plants such as basil and allspice when it chews their leaves and extracts the smelly substances. The bee pollinates a wide variety of local plants, which reciprocate with nectar rather than with an aphrodisiac. Once again, the insect has more freedom of action than does its partner.

  As a result, the two parties are often less entangled than Darwin imagined. A shift in one is not always matched by an equivalent move by the other, with deeper flower trumped by longer tongue. Molecular trees of plants and pollinators suggest that the insects have instead often switched to species with shallower flowers from which nectar can be sucked with less effort.

  The orchid’s ability to force its ally to serve its selfish interests is further limited because such gorgeous beings are often rare and scattered among other species. Make life too hard and the insect will sip elsewhere. Infidelity by the pollinator is bad news for the orchid as it may fail to export its own genes and in addition it may get pollen from the wrong species. Nevertheless, not all the pollinators have been promiscuous, for fossil water lilies from ninety million years ago have flowers quite like those of their modern ancestors as evidence that their association with beetles is ancient indeed.

  The pressure for sex often causes natural selection to run away with itself. Like many showy animals, birds and butterflies included, there are lots of different orchids. Twenty-five thousand kinds are known, compared with no more than a hundred or so species of wild roses (which are happy to attract almost any insect that might pass by). Most of the barriers to gene exchange among the orchids are held in the brains of their pollinators. As a result, the fertile minds of gardeners have been able to generate thousands of hybrid forms by getting round the ancient bond between flower and insect with a simple paintbrush. Their success shows how fine the balance of barriers to the movement of DNA must be. A tiny shift can change the equation of flower and pollinator and make a new species. In some cases a mutation that changes colour from a hue attractive to bees to another favoured by birds has started a new species in a single step. In the same way, in orchids pollinated by scent-seeking bees, a subtle shift in the proportions of each constituent can attract different kinds of bee, which means that physically identical plants may in fact be distinct entities that never exchange genes.

  Orchids bolster Darwin’s case that species arise through the action of natural selection and he soon realised that their diversity had been driven by the vagaries of insect behaviour. He was much less certain of the origin of flowers themselves, which he called ‘an abominable mystery’ and a ‘perplexing phenomenon’. The mystery has been cleared up and the orchids have helped.

  Plants colonised the land more than four hundred million years before the present. Those pioneers had no flowers and neither did the huge forests of giant ferns that covered large parts of the planet a hundred million years later. The fern forests declined and the dinosaurs flourished for an age in a flowerless world. Not until the first flowers of all, perhaps a hundred and fifty million years ago, did the conflict between insect and plant begin. It led to an explosion of change in both parties. Their joint transformation was spectacular, for more than three hundred thousand species of flowering plants have evolved, together with several times that number of insects.

  The oldest fossil flower comes from a famous bed close to the estuary of the Yellow River in China. It dates from around a hundred and twenty-five million years ago, at the time when the white cliffs of Dover were being formed in a shallow sea. It looked rather like a water lily and floated in fresh water with its small flowers above the surface. For tens of millions of years such structures remained modest, but sixty-five million years ago - just as the dinosaurs left the stage - the world burst into bloom.

  The orchids played their part in beautifying an unpeopled world. A distinctive pollen sac attached to a stingless bee has been found in twenty-million-year-old amber from the Dominican Republic. That orchid’s modern relatives use just the same group of insects to transfer their male cells. The molecular clock suggests that orchids as a whole originated around the time of the extinction of the dinosaurs. Their massive radiation happened just after that memorable event and was accompanied by parallel change in the insects that pollinate them.

  The great blooming was evidenc
e of an early skirmish in the war between orchid and insect. Conflict between plants and pollinators has gone on ever since. It is expensive and never more so than when it escalates. The Soviet Union collapsed under the financial pressures of its attempts to match the power of the Americans and for centuries Britain and France spent a third of their wealth in mutual conflict. In war, as in love and business, lavish display is a test of merit. A military parade intimidates the enemy and a costly publicity campaign is a sign of a high-class company. The medium becomes the message, the powerful stay in charge, cheats go bankrupt and, for most of the time, truthful ostentation prevails. The best signals are too expensive to copy, which is why McDonald’s sues anyone who imitates their golden arches and why Japanese Yakuza gangsters cut off their fingers.

  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 ri
ght 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.