Darwin's Island Part 7

Pollination has attracted attention since ancient times. Both Aristotle and Virgil were interested in bees, but only because they made honey (or collected the stuff, for the Greeks imagined that it fell from the air: 'air-born honey, gift of heaven') rather than because they were essential for reproduction. The Egyptians, in contrast, understood that dates would not grow on cultivated palms unless male flowers were shaken on to the females. They used their slaves as pollinators. A diversity of other creatures has been called in to act as marital aids and quite often that duty drives their own evolution. Two hundred thousand insects (the male malaria mosquito included) are known to transfer pollen and their own vast radiation into a variety of forms began soon after the origin of flowers. From the tropics to the sub-Arctic, hundreds of species of bird are busy shifting genes. Some, such as humming birds, can almost never afford to stop as they need a constant supply of nectar to keep their tiny bodies at a high level of activity. Mammals are also involved, and a certain Ecuadorian bat has a tongue half as long again as its own body - in relative terms the longest of all mammalian tongues. It is coiled up in a special cavity in its chest, except when the animal is feeding. An African tree is even adapted for pollination by the giraffes that browse upon its leaves. In Australia, too, marsupials have taken up the job for the honey possum has lost many of its teeth and gained a long tongue. The sugar glider - a marsupial that floats through the air from flower to flower - is much the same.

Plants want their go-betweens to be cheap, trusty and eager, while pollinators would prefer to be fat, wanton and as idle as possible. The flower shows that a reward is on offer while the other party must decide whether the hard work needed to get it is worthwhile. The struggle between the two parties leads to the evolution of displays that dwarf the efforts of any animal. A bunch of flowers is an advertis.e.m.e.nt - a silent scream from the s.e.xually frustrated. Like all advertis.e.m.e.nts it attempts to rea.s.sure those who see it that a high-quality product is on view. In commerce, as in life, the temptation to cheat is never far away; to make false promises with no reward, or to take the prize and fail to complete the task.

Plants and animals make signals of many kinds. They advertise their qualities as a mate, their willingness to fight for territory or food, or their ability to escape from a predator who might as a result be dissuaded from bothering to attack. One surprise is that the signals are so often honest when the reward for dishonesty is so high, be it in the form of s.e.x, food or safety. Some signs are direct and impossible to fake: large tigers make scratch marks higher up a tree trunk than can their smaller rivals and can as a result hold bigger territories. Often, though, the information is indirect. Thus, a black and yellow wasp warns predators about its dangers without the need to sting all of them.

Such secondary signals, too, are sometimes pricey and hard to simulate. Giant antlers, vivid tails or spectacular blooms can be made only by those who can afford them: the healthiest, the s.e.xiest or the super-aggressive. Most of what we interpret as the joys of nature costs a lot, for a stag may die in battle, and a male nightingale loses a tenth of its body weight after a night spent singing in the hope of s.e.x. Testosterone itself, that signifier of masculine ident.i.ty, is costly in many ways. It suppresses the immune system, so that a red deer male in s.e.xual frenzy is open to attack by parasites - and if he can keep roaring in spite of his tapeworms he might have particularly fine genes. Elephants go even further. Now and again, one falls into a state of 'musth', in which its testosterone level goes up by fifty times. The agitated beast becomes very aggressive, and a small animal will fight even to the death against a larger rival.

Flowers, too, are not cheap. Orchid fanciers pay tens of thousands of dollars for prize specimens and the trade as a whole has a worldwide turnover of several billion. The orchids themselves invest far more of their limited capital into s.e.xual display than does the most avid gardener, for if they do not their genetical future is over. The cost of s.e.x to each orchid and to those that market them is manifest in the fact that, in the world of the garden centre, many of the specimens are grown from cells in culture rather than by persuading the plants to go through the expensive ritual of s.e.x.

Orchids and other flowers are, like the peac.o.c.k's tail, animated billboards that advertise s.e.xual prowess. For all signals, two parties are involved: those who transmit a message and those who receive it. A system of checks and balances tests whether the information is accurate; that those with the biggest antlers or brightest blooms really are the fiercest or most generous. The system is always under test by potential fraudsters at both ends and sometimes cheats get in. Often, they do well. For insects, black and yellow is no more difficult to manufacture than is brown or blue - and a whole group of harmless flies does just that, with bright stripes that make a false claim of a waspish nature. That costs the wasps a lot when a hungry bird attacks under the a.s.sumption that the pattern advertises good taste rather than potential danger.

Such swindlers also flourish in the botanical world - and in orchids most of all. To his considerable surprise, Charles Darwin found that among those elegant flowers dishonesty pays. Many of his specimens had gorgeous displays, but gave no payment to their pollinators. He found it hard to believe that Nature could be so fraudulent or that insects were so foolish as to fall for 'so gigantic an imposture' and suggested, wrongly, that his plants had an as yet undiscovered reward. His finding throws light on a question that he posed but failed to solve: how can natural selection favour the dishonest? The orchids give part of the answer.

The battle for s.e.x is a war of all against all. It may end in an arms race; a tactical struggle in which every move made by one party is countered by the other. Sometimes, as in the Cold War, each antagonist is forced into ma.s.sive investment, and, as in those days, negotiation may end in stalemate. To an untutored eye that may look like peace, but it is in truth no more than battle deferred. The orchids, beautiful as they are and exquisite as their adaptations to the needs of their pollinators might be, show such a struggle hard at work and show how propaganda - false information - is useful in both love and war.

Many of Darwin's own observations were made on the 'Orchis Bank', close to his home, where he found eleven species of the plants. As he noted with a certain pride, 'no British county excels Kent in the number of its orchids', but he also studied specimens sent from all over the world. He soon saw how the conflict between plant and pollinator had led to change. He speaks of an orchid, 'the Angraec.u.m sesquipedale Angraec.u.m sesquipedale, of which the large six-rayed flowers, like stars formed of snow-white wax, have excited the admiration of travellers in Madagascar'. It had 'a whip-like green nectary . . . eleven and a half inches long, with only the lower inch and a half filled with very sweet nectar. What can be the use, it may be asked, of a nectary of such disproportional length? . . . in Madagascar there must be moths with probosces capable of extension to a length of between ten and eleven inches! . . . As certain moths of Madagascar became larger through natural selection in relation to their general conditions of life . . . those individual plants of the Angraec.u.m which had the longest nectaries . . . and which, consequently, compelled the moths to insert their probosces up to the very base, would be fertilised. These plants would yield most seed and the seedlings would generally inherit longer nectaries; and so it would be in successive generations of the plant and moth. Thus it would appear that there has been a race in gaining length between the nectary of the Angraec.u.m and the proboscis.' In 1903, that long-tongued insect, product of an endless contest with its plant, was at last discovered and named as Morgan's Sphinx Moth. A long conflict of interests had forced both parties to adapt themselves to each other's demands.

As the sage of Down House collected orchids from the fields and heaths around his comfortable home and examined the specimens sent to him from afar, he became more and more impressed by the ingenuity of the ways in which as they pa.s.s on pollen: 'Hardly any fact has struck me so much as the endless diversities of structure, - the prodigality of resources, - for gaining the very same end, namely, the fertilisation of one flower by the pollen from another plant.' He glimpsed but a small part of the game played by all plants as they fulfil their s.e.xual destiny.

As Darwin showed, nine years after the orchid book, in The Descent of Man, and Selection in Relation to s.e.x The Descent of Man, and Selection in Relation to s.e.x, a male peac.o.c.k's flashy rear says nothing about the merits of tails, but a lot about his status as a high-quality mate who can afford a gorgeous adornment. The same is true of plants. More food allows them to make more blooms and to proclaim their excellence to a larger audience. To remove a few flowers may also allow them to grow more fruits, as proof of how expensive it is to be attractive. The brightest and most generous individuals get more pollinators and pa.s.s on more of their genes, which promotes yet more brightness and generosity in the next generation and, almost as an incidental, leads to an outburst of diversity as the balance of s.e.xual advantage species in different lineages.

Orchids belong to the great subdivision of the flowering plants that generates just a single leaf as the seed germinates. It contains the gra.s.ses (crops such as rice included), bananas, tulips and more. The orchids themselves are among the largest families of all for only the group that contains daisies and sunflowers possesses more species. Around twenty-five thousand different kinds are known - about an eighth of all plants with flowers - and no doubt many more remain to be discovered. Britain has just forty-six native kinds, several of which are rare.

Because orchids are so attractive they are important in the conservation movement (and cynics call them 'botanical pandas'). They may look fragile but many are tough. Their capital lies in the wet and cool hill-forests of the tropics, and a third of all known species are found in Papua New Guinea. Plenty more live in the Arctic or in temperate woodlands, fields and marshes. They grow on the ground or high in the branches of trees, or on rocky slopes and gra.s.slands. A few live underground and never see the light of day. In some places the plants are short of water and, like cacti, develop thickened stems or tubers to store a reserve. Some have leaves as big as their relatives the bamboos while a few are parasites with almost no foliage at all. Others, such as the vanillas, make vines twenty metres long. Some kinds are tiny, with a flower head that would fit on the head of a pin, while the flower of a certain tree-dweller from New Guinea is fourteen metres around and weighs about a thousand kilograms (a specimen caused amazement at the Great Exhibition in 1851). Plenty of others have multiple displays several metres long. A few have opted out of the endless and expensive conflict and are pollinated by the wind while one Chinese kind has abandoned the whole business of s.e.x and indulges in a strange internal dance in which its male element curves backwards and inserts itself into its own female orifice.

Some of the flowers are simple. They are dark and look rather like the entrance to a burrow, which attracts a bee to come in for a snooze and pollinate as it does so. Many others use far more elaborate tactics. Some are perfect six-pointed stars while others resemble a gla.s.s-blower's nightmare with fine tendrils that hang together in delicate and lurid bunches. Yet others look as if they are moulded from thick pink plastic. The flowers are scarlet, white, purple, orange, red or even blue. One species is pollinated by a wasp. It generates a chemical identical to that emitted by a leaf chewed by grubs - the wasp's favourite food. The wasp as it visits gets not a meal of tasty flesh, but a load of unwanted pollen. For those over-impressed by the beauties of botany, certain orchids smell like putrid fish to attract carrion-feeding flies.

The biological war between flower and insect, like the whole of evolution, involves an endless set of tactics, but no strategy. It has produced a vast variety of blooms, each of which evolved in a manner that depends on the preferences of their pollinators and on what turns up in the form of mutations. Darwin noted what strong evidence the orchids were against the then common notion that the beauties of nature emerged from some kind of plan: their structures 'transcend in an incomparable degree the contrivances and adaptations the most fertile imagination of the most imaginative man could suggest'. They were another weapon in the battle against the idea of design, a 'flank movement on the enemy'.

However remarkable the details, all their flowers are based on the same fundamental plan. It resembles that of the distantly related, but simpler, lily (and Goethe himself, with his interest in botany, described orchids as 'monstrous lilies'). The parts are arranged in threes, or multiples of that figure. The central lobe is often enlarged into a coloured lip which acts both as a flag to attract insects and as a landing strip that allows the visitors to reach the sweet reward at its base. Often, the flower rotates to turn upside down as it develops. The male organ sits at the end of a long column and the male cells, the pollen, are not powdery as in other plants but instead are held together in large ma.s.ses, with up to two million minute grains in each. They are covered with a sticky secretion that can attach the whole lot to an insect. The female part lies deeper within, on the same column as the male. Once fertilised, the orchid may produce thousands of tiny seeds in every capsule - no more than a minute proportion of which have any hope of success.

When the pollinator enters, some means is found to attach male s.e.x cells to it. Many orchids have a spring-loaded mechanism that fires a ma.s.s 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 ma.s.s 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 ma.s.s 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 ma.s.ses 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 s.e.x lives have come to depend upon them. They obtain their s.e.xual 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 s.e.xual mix transmitted to pockets in the bees' hind legs. The habit evolved from the insects' ancient habit of marking their s.e.xual 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 s.e.xual 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 a.s.sociation with beetles is ancient indeed.

The pressure for s.e.x often causes natural selection to run away with itself. Like many showy animals, birds and b.u.t.terflies 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 pa.s.s 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 const.i.tuent can attract different kinds of bee, which means that physically identical plants may in fact be distinct ent.i.ties 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 ma.s.sive radiation happened just after that memorable event and was accompanied by parallel change in the insects that pollinate them.

The great blooming was evidence 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-cla.s.s 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 j.a.panese 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-cla.s.s 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 inst.i.tution 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 n.o.bel 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 s.e.x 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 s.e.xual scent. The male bees or spiders - understandably - try to copulate with their spurious brides and in their failed attempt to pa.s.s 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 s.e.x, 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 s.e.x 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 l.u.s.t, of their visitors. They advertise not s.e.x 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 a.s.sistant 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 a.s.sociations 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 s.e.xual dishonesty that has emerged since Darwin's day. When it comes to the need to pa.s.s 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 s.e.xual 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 s.e.xual 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 ma.s.s 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 pa.s.s 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 p.e.n.i.s longer than its own body.

s.e.xual 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 s.e.xual 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 cla.s.sic 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 s.e.x before marriage disrupts brain chemistry and leads to divorce. The hormone, he says, is 'G.o.d'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 s.e.xual 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 s.e.x outside the household. Voles are socially faithful, but s.e.xually 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 s.e.xual 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 s.e.xual 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 n.o.bleman 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 s.e.xual 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.

In fact, such suspicions are misplaced. Surveys of on-line daters show impressive levels of accuracy in their descriptions of themselves, for almost all say something close to the truth about age, body build, wealth, education, politics, marital history and more (admittedly, men tell slightly more lies about their income and women about their weight). The daters disapprove strongly of anyone who did not live up to their claims on a first meeting and swore that they would go no further with them. Deception is not an effective s.e.xual strategy. For men and women, honesty pays and the fraudulent are rejected as partners as soon as they are detected.

In the dating game, on the other hand, there are few disappointments that a bunch of orchids will not put right.

CHAPTER IX.

THE WORMS CRAWL IN.

The fields of Britain are criss-crossed by earnest men with metal-detectors. Despised by archaeologists for the damage they cause, the 'discoverists', as they call themselves, have found thousands of coins, swords, belt buckles and the like. Some of the objects were hidden, or buried by their owners in times of danger, but most simply sank from sight. Why?

Charles Darwin, as usual, got it right. The past had been entombed by worms. He hymns their praises in his last book, The Formation of Vegetable Mould, through the Action of Worms, with Observations on their Habits The Formation of Vegetable Mould, through the Action of Worms, with Observations on their Habits: 'The plough is one of the most ancient and most valuable of man's inventions; but long before he existed the land was in fact regularly ploughed, and still continues to be thus ploughed by earth-worms. It may be doubted whether there are many other animals which have played so important a part in the history of the world.' His literary swansong discusses the anatomy and habits of such creatures, their intellectual life (such as it is) and, most of all, their ability to disturb the surface of the Earth, to aerate, turn over and improve the soil, and to sink any object that lies upon it. At the time its author claimed that he had produced no more than 'a curious little book' on a matter that 'may appear an insignificant one', but the ravages of the plough since it was invented thousands of years ago and the damage done to the surface of our planet by today's agriculture mean that the work of the worms is crucial not just to the history of the world but to its future.

The power of such small beings to seal the fate of objects far larger than themselves shows, once again, the huge consequences that can emerge from what may appear to be the trivial efforts of Nature. Darwin was aware of the potential of the worm as proof of the might of slow change; as he said of their efforts: 'the maxim de minimis non curat lex de minimis non curat lex does not apply to science'. They were the final test of his obsession with the c.u.mulative potential of the small and he was proud of his results. He dismissed the arguments of a Mr Fish, who denied the animals' talents, as 'an instance of that inability to sum up the effects of a continually recurrent cause, which has often r.e.t.a.r.ded the progress of science, as formerly in the case of geology, and more recently in that of the principle of evolution'. does not apply to science'. They were the final test of his obsession with the c.u.mulative potential of the small and he was proud of his results. He dismissed the arguments of a Mr Fish, who denied the animals' talents, as 'an instance of that inability to sum up the effects of a continually recurrent cause, which has often r.e.t.a.r.ded the progress of science, as formerly in the case of geology, and more recently in that of the principle of evolution'.

The elderly savant's attraction to such creatures had started long before he thought of science. In his autobiography he notes that, as a child, he had been so upset by their contortions when impaled on fish-hooks that, as soon as he heard that it was possible to euthanise them with salt and water, he never again 'spitted a living worm, though at the expense, probably, of some loss of success!' His later studies introduced a new world beneath our feet, gave life to the idea of animals as a geological force and, as an incidental, showed how even simple animals have a rich mental life of their own. His work became the foundation of a science which has now, almost too late, noticed the dire state of the world's vegetable mould and has begun to do something about it.

In 1837, just a year after the Beagle Beagle voyage, Charles Darwin presented a paper on worms to the Royal Geological Society. Later he published a few notes on the subject, which occupied him at odd moments for forty years. At last, at the age of seventy-two, he wrote voyage, Charles Darwin presented a paper on worms to the Royal Geological Society. Later he published a few notes on the subject, which occupied him at odd moments for forty years. At last, at the age of seventy-two, he wrote Vegetable Mould Vegetable Mould, which was published at nine shillings in 1881, just six months before his death. The book was received with what he called 'almost laughable enthusiasm' and sold nearly as many copies in its first few years as had The Origin. The Origin.

Soil is where geology and biology overlap. Adam's name comes from adama adama - the Hebrew for soil - and Eve from - the Hebrew for soil - and Eve from hava hava, or living: an ancient statement of the tie between our own existence and that of the ground we stand on ('h.o.m.o' and 'humus' also share a root). The epidermis of the Earth is no more than around one part in twenty million of its diameter while our own skin, in contrast, is about a five-thousandth as thick as the average human body. Leonardo da Vinci wrote that 'We know more about the movements of the celestial bodies than of the soil underfoot', and until Vegetable Mould Vegetable Mould that was still almost true. that was still almost true.

Since then, earthworms and their relatives have been studied by geologists, ecologists, molecular biologists and many others. Archaeologists, too, have reason to be grateful for their efforts, for without the animals our insight into history would be far less complete than it is, for most of the evidence left by our ancestors would not be buried but washed away. More important, perhaps, without worms we would starve.

Vegetable Mould built upon an observation Darwin had made as a young man. Twelve months after his return to his native island from his famous voyage, he visited his uncle - and future father-in-law - Josiah Wedgwood, at Maer Hall in Staffordshire. Wedgwood took him to a field upon which had been scattered, fifteen years earlier, a ma.s.s of lime, cinders and burnt marble, the detritus of his Etruria pottery works nearby. The material had, over that period, been covered by a layer of earth. Wedgwood suggested to his nephew that perhaps worms had done the job. The young scientist agreed, but saw this at first as little more than a 'trivial gardening matter'. In time, as the notion that - for both rocks and flesh - small means could give rise to large ends grew in his mind, he saw in those humble creatures a real chance to experiment on the measured actions of Nature. built upon an observation Darwin had made as a young man. Twelve months after his return to his native island from his famous voyage, he visited his uncle - and future father-in-law - Josiah Wedgwood, at Maer Hall in Staffordshire. Wedgwood took him to a field upon which had been scattered, fifteen years earlier, a ma.s.s of lime, cinders and burnt marble, the detritus of his Etruria pottery works nearby. The material had, over that period, been covered by a layer of earth. Wedgwood suggested to his nephew that perhaps worms had done the job. The young scientist agreed, but saw this at first as little more than a 'trivial gardening matter'. In time, as the notion that - for both rocks and flesh - small means could give rise to large ends grew in his mind, he saw in those humble creatures a real chance to experiment on the measured actions of Nature.

Darwin continued to study the animals as he travelled across England with his wife and children. They were not the only tourists of those days. The Victorians were fond of excursions, and many were, like the modern discoverists, anxious to cart off relics for their own delight. In 1877, in a brief respite from ill health, Charles took his wife to visit Stonehenge. He dug pits around several of the 'Druidical stones', as the monoliths were then called, and noted that even the largest had been sunk several centimetres deep by the worms. Emma worried that her husband might have sunstroke as he sported with the relics, and she recorded her conversation with the site's guardian, 'an agreeable old soldier'. 'Sometimes,' the venerable trooper told her, 'visitors came who were troublesome, and once a man came with a sledge-hammer who was very troublesome to manage.'

A few years earlier a hammer and chisel had been provided at Stonehenge for the use of those who wanted a curio of ancient times. Their intellectual descendants still agitate the nation's soil. A hobby that began with chunks chipped off monuments has become an electronically powered craze, with, at its peak, almost two hundred thousand enthusiasts in Britain (they include Bill Wyman of the Rolling Stones, who markets his own metal detectors for 'Treasure Island UK'). For a time the 1960s Prime Minister, Harold Wilson, was an honorary patron of the detectorists' organisation. The numbers are well down from those frenzied days and in most of Europe the practice remains illegal, but in 1997 the British government bowed to reality and changed the law to reward those who report their finds; they are, said the minister for culture of the time, 'the unsung heroes of the UK's heritage'. The Portable Antiquities Scheme, as it is called, applies to England and Wales alone, for Scots must still give up their treasures to the Crown. South of the Border, the number of objects reported has risen from fewer than a hundred per year to thousands. The scheme now lists more than three hundred thousand items. Recent triumphs include the discovery of a four-thousand-year-old gold cup at Ringlemere, in Darwin's home county. Its finder shared a 250,000 reward.

The Ringlemere cup was concealed by men anxious to placate the G.o.ds but many other objects have been hidden by humbler creatures with simpler motives. Electronic sweeps of the fields around Down House reveal many coins, necklaces, buckles and the like. Vast numbers more remain, no doubt, to be uncovered. They were buried by worms as they searched for shelter and for food.

The earthworm has undoubted charm. It belongs to a group known as the annelids, which include the leeches and lugworms and is related to less agreeable creatures such as the parasites that cause elephantiasis in tropical Africa. The creatures are more distant kin of snails and slugs. Their ancient roots are best revealed by patterns of DNA similarity, as soft-bodied creatures do not leave many fossils (even if the remains and the tracks of a few primitive annelids are found as far back as the Cambrian). Today, three thousand or so species are known, and, given our ignorance of tropical nature, many more must remain to be found. Most are small and una.s.sertive, but a certain Australian kind grows to three metres long and ejects a jet of fluid half a metre into the air when annoyed. Britain has a just over a couple of dozen sorts while France has six times as many. A rain forest has far more.

A 2005 survey at Down House, in the woods by the famous Sandwalk - the site of its owner's regular stroll - and in a nearby meadow in which Darwin had noted that stones were soon buried by worms, revealed that his home was still a hotbed for the creatures. Nineteen of the twenty-eight British species were found there or nearby. The most abundant species nowadays, and no doubt in Victorian times, was the black-headed worm, which is smaller than the familiar lobworm found in city gardens and used as bait by fishermen. The animals were most abundant in the kitchen garden, probably because of its many decades of fertiliser and a strict ban on pesticides.

A worm is an animated intestine. The body is divided into segments, each with an outer layer of muscle that encircles it and an inner muscle sheet that runs parallel to the axis. Each segment bears a simple kidney with a series of even simpler hearts distributed along the animal's length. The body is hollow and filled with fluid and down the centre runs a long digestive tube. Many species have internal glands filled with lime - calcium carbonate. Some have coloured blood while others are almost transparent. Certain kinds smell of garlic, perhaps to put off predators.

The skin is covered with stiff spines that help the creature move through the soil as it eats its way onwards, pumping out waste from the rear end as it goes. In some kinds, the slime made as it burrows hardens into a solid wall that keeps a track open for a possible return while in others the soil collapses behind the questing worm as it travels. Some worms live on or just below the surface and in leaf litter, while others hide deeper, sometimes six metres down. A few prefer rotten wood. Those most important to farmers roam the top metre or so of soil. Some species reuse their burrows while others set out instead to build new homes. The common lobworm makes a single excavation, with one or two branches, while others make a network with several exits.

Most earthworms spend most of their time at rest in their underground fortresses and venture forth only when conditions are suitable. In winter they dig down and hibernate and in dry summers build a coc.o.o.n in which to rest until the rains come. After a downpour, they can travel in vast concourses across the surface. Darwin noted that many species do not like to leave the doors to their burrows open, and sealed them by pulling in leaves. Others made piles of digested earth - casts - on the ground, and in some tropical forms these could be several centimetres high. The creatures excrete with some care, for the tail, he noted, was used almost like a trowel to make a neat heap of ordure. A careful look at the body waste revealed many fine grains of silt that had been broken down from larger particles within the soil.

Worms live for no longer than two years or so, and most die younger than that. They get us all in the end, but some creatures get their retaliation in first. Many animals eat them. Badgers and hedgehogs are fond of a diet of worms, and as Alfred Russel Wallace had noticed, the natives of South America appreciated them too. In the Orinoco Basin of Venezuela smoked earthworms still form an important part of the local Indians' cuisine.

Many species regenerate their tails when cut off, and a few do the same for a head, but - in spite of myths to the contrary - none of the familiar kinds can develop into two individuals when cut into pieces (an amputated tail may grow a mirror image of itself, but then it starves). A few do reproduce by simple fission; the back breaks off and forms a new worm, and - in some - the animal splits into a dozen or more pieces, each of which gives rise to a new individual. The ability to multiply by breaking into fragments is common in the lower reaches of the animal kingdom, but the worms are the most advanced creatures to possess that talent.

The s.e.x-life of annelids is varied indeed. Several are all-female and lay eggs without benefit of males. Some of the clonal kinds spread fast and have invaded new habitats such as sewer pipes. Others are hermaphrodites, with separate male and female genitalia. s.e.x happens in a long slime tube in which boy-girl meets girl-boy. The two animals lie head to tail to consummate their relationship. The male checks the virginity or otherwise of the female element of its partner and adjusts the amount of sperm to match. It increases the volume by three times when it senses that its mate has already had s.e.x with another, no doubt to flood out the previous donation. The animals prefer to copulate underground, but sometimes move to the surface (in Darwin's words, 'their s.e.xual pa.s.sion is strong enough to overcome for a time their dread of light'). A swollen mid-section of the body forms a protective coc.o.o.n as the eggs are laid.

Worms are among the simplest creatures to have a central nervous system, with a distinct brain connected to a set of nerve cords (although even after the brain has been removed the animals can mate, feed and find their way through a maze). A section of the worm book is headed 'Mental Qualities' - but its first sentence reads 'There is little to be said on this head.' Even so its author set out to see just what their lowly wits were capable of. He noted that they often pulled in leaves to seal the mouth of the burrow, perhaps, he thought, to protect themselves from the cold. Whatever crosses the animal's mind as it drags fronds into its home, it acts with a degree of foresight. Worms, he found, prefer to grasp a leaf by its tip. More than nine-tenths of broad leaves were pulled in from that end, but for narrower kinds, which are easier to slip into a small opening, just two in three. Those of the rhododendron curl up when on the ground, so that some were narrower near the base, and others near the tip. The creatures, more often than not, pulled them in by the narrow end. They were just as smart when it came to pine needles, which could be dragged in only base-first.

Darwin admired such rationality, for it forged a link between the lowest creatures and the most n.o.ble: 'one alternative alone is left, namely, that worms, although standing low in the scale of organization, possess some degree of intelligence'. In the first real experiment on invertebrate psychology Charles and his son Horace presented the animals with paper triangles cut into various shapes - and once again they acted in the most efficient way, for on most occasions they seized the pointed end. Other studies of their intellectual universe involved the choice of foods - meat, onions, starch or lettuce (with beads and paper used in an attempt to trick them). In a series of midnight expeditions to the lawns of Down House, the father-and-son team shone lamps upon the animals, warmed and cooled them, and subjected the unfortunate creatures to tobacco smoke. The subjects were 'indifferent to shouts' and just as unconcerned by the shrill notes of a metal whistle or the deep tones of a ba.s.soon. They did respond to vibration, and became agitated when placed on top of a piano. They were 'more easily excited at certain times than others', and a series of taps upon the ground made them emerge. Hungry birds could often be seen doing just that to persuade their prey to venture forth. There was, no doubt, a wide gap between their mental world and that of the naturalist - but profound as it was, it had been bridged by the same system of slow change that moulded the physical universe of each.

Those patient experiments on the inner life of the burrowers were an introduction to their wider role in the world of the soil and their ability to modify their own habitat and that of those who stride the ground above. Most of Darwin's book is devoted to the animals' impressive ability to disturb and fertilise the ground.

That talent had been noticed long before. Aristotle described the worms as the 'Earth's entrails'. Cleopatra herself decreed them to be sacred animals, and established a cadre of priests devoted to their welfare (although they were less important than scarabs, those other recyclers of dung, whose image was universal in Pharaonic times). Cleopatra's interest arose because the creatures were so important to the fertility of the mud laid down by the Nile (and they were also useful in weather forecasting). Herodotus knew as much when he wrote that 'Egypt is the gift of the Nile', and most of the immense deposit of the great river that comes down in the annual flood does indeed begin as eroded worm-casts from the Ethiopian highlands, far upstream. The same is true closer to home. In 1777, the English naturalist Gilbert White wrote, in a letter unknown to Darwin, of their 'throwing up infinite numbers of lumps of earth called worm-casts which, being their excrement, is a manure for grain and gra.s.s . . . the earth without worms would soon become cold, hard-bound and void of fermentation, and consequently sterile'. As he put it in The Natural History of Selborne The Natural History of Selborne, 'Earth-worms, though in appearance a small and despicable link in the Chain of Nature, yet, if lost, would make a lamentable chasm.'

Without their help, we would ourselves fall into a real abyss. Those simple creatures play a role in both economics and history. They improve drainage and break organic matter into fine particles: 'all the vegetable mould over the whole country has pa.s.sed many times through, and will again pa.s.s many times through, the intestinal ca.n.a.l of worms'. That unromantic product determines the fertility of the soil, which does a lot to dictate the nature of the society that lives upon it.

In the mid-nineteenth century gardeners saw the animals as mere pests, relatives of tapeworms and such unpleasant beasts (the word vermin, indeed, has the same Latin root as does 'worm'). Books advised how to get rid of the unwelcome visitors by driving them from their burrows with mallets, poison or steel rods inserted into the ground and played with a bow (a pastime known as 'worm-grunting' to the American fishermen who still use it to collect bait). Soil was considered to be a product not of biology but of chemistry and physics, for it came from the mechanical dissolution of rock and the chemical decay of vegetation. The Comte de Buffon, mentioned in The Origin The Origin as a pioneer of the notion of natural selection, was, like his British successor, interested in what made the Earth's outer cloak. He noted that many soils contained grains of minerals such as iron, and that cover tends to be thinner on mountain slopes than in valley floors. All this was, he claimed, proof of the breakdown of rocks and the importance of rain, rivers and gravity in disturbing the surface. The Russians of the period - obsessed as they were with the vastness of the steppe and its effect on the Slavic psyche - were pioneers in the study of the deep and dark as a pioneer of the notion of natural selection, was, like his British successor, interested in what made the Earth's outer cloak. He noted that many soils contained grains of minerals such as iron, and that cover tends to be thinner on mountain slopes than in valley floors. All this was, he claimed, proof of the breakdown of rocks and the importance of rain, rivers and gravity in disturbing the surface. The Russians of the period - obsessed as they were with the vastness of the steppe and its effect on the Slavic psyche - were pioneers in the study of the deep and dark chernozem chernozem, the 'black earth' that fed the ma.s.ses and nourished the nation's soul. They, too, emphasised the role of chemical decay. Why should such mundane creatures as worms play any part in the sacred soil of Mother Russia?

Physics and chemistry do, no doubt, help build the ground beneath our feet. Chalk and limestone dissolve in the rain and even sandstone and granite can be eroded away to make earth. Tiny cracks fill with water, which shatters rock when it freezes. The surface tension that holds water to the walls of minute channels also exerts huge pressure as the liquid warms and cools. Clay itself - little more than tiny particles of ground rock - is a product of such insidious action.

The earliest fossil soil is three thousand million years old, almost as ancient as land itself. It was made with no help from biology. Three hundred and fifty million years before the present the first land plants moved on to a sterile landscape. Since then, life has fed on soil and soil on life, in a great cycle that enriches both.