Climbing Mount Improbable

by Richard Dawkins

  In some species, the fig contains two kinds of female flowers, long-styled and short-styled. (The style is the spiky female part that sticks up in the middle of any flower.) The wasp tries to lay eggs in flowers of both kinds but her ovipositor is too short to reach the base of the long-styled flowers so she gives up and moves on. Only when she connects with a short-styled flower does her ovipositor hit bottom, and she lays one egg. In other species of fig which lack the distinction between long-styled and short-styled flowers, the fig tree's method of policing wasp behaviour can be more draconian. Or so believes W. D. Hamilton, now my Oxford colleague and one of Darwin's foremost successors today. Hamilton suggests, with some support from his {304} own observations in Brazil, that fig trees can detect when a fig has been over-exploited by wasps. Figs that have eggs laid in all their flowers are useless from the tree's point of view. The wasps have been too selfish. They have killed the goose that lays golden eggs. Or rather, according to Hamilton, the goose commits suicide. The fig tree causes an over-exploited fig to drop to the ground where all the wasp eggs inside perish. It is tempting to see this as revenge, and there are theoretically respectable mathematical models which could free us from the suspicion of anthropomorphism. But in this case probably what the tree is doing is not so much wreaking vengeance as cutting its own losses. It costs resources to ripen a fig, and resources are wasted if used to ripen a fig ruined by greedy wasps. This kind of strategic game language, by the way, in which we are not afraid to use words like ‘revenge’ and ‘policing’, will recur throughout this chapter. It is legitimate if handled properly, which will often turn out to mean using the mathematical theory of games.

  Returning to the life cycle of the typical fig wasp, our female had just wriggled like Alice through the tiny door, never to see the outside world again, and she set about relieving herself of the pollen she had gathered in the fig of her birth. The pollination behaviour of female fig wasps has a form which makes it seem deliberate. Far from letting the pollen be accidentally brushed off her body, as happens with most pollinating insects, the female of at least some species of fig wasp unloads her cargo with the same industry and attention that she lavished on loading up. She again uses the brushes on her front legs, systematically shovels pollen out of her custom-made pockets on to the brushes, and vigorously shakes it on to the receptive surface of the female flower.

  By laying her eggs in female flowers the female wasp brings our story of the life cycle to its close. Her own life is over, too. She crawls to some damp crevice of the enclosed garden and dies. She dies, but she leaves behind megabits of genetic information faithfully recorded in her eggs, and the cycle resumes.

  Give or take a few details which I'll enlarge on in a moment, the story I have told is similar for most kinds of figs. Ficus, the fig genus, is one of the largest in the living kingdoms. It is also a very diverse genus. In addition to the two species of edible (by us) figs, the genus {305}

  Figure 10.3 (a) strangler fig; (b) baobab tree entwined by strangler fig.

  includes the rubber tree, the sacred banyan tree, the Bo tree Ficus religiosa, under which the Buddha contemplated, various shrubs and creepers, and the sinister ‘strangling’ figs of the tropics. The story of the strangling figs is worth telling. The forest floor is a dark place, starved of solar energy. It is the goal of every tree in the forest to reach the open sky and the sun. Tree trunks are leaf-elevators, devices for lifting solar panels — leaves — above the shade of rival trees. Most trees are fated to die as saplings. Only when an adult tree in the immediate vicinity crashes down, overcome by gales and years, does a young sapling have its chance. At any one point in the forest, this lucky event may happen just once in a hundred years. When it does, there is a gold rush to the sun. All the saplings in the area, drawn from many species, enter a headlong race to be the one to fill the precious gap in the canopy. {306}

  But the strangling figs have discovered their own sinister short cut and their story would upstage the serpent of Genesis (Figure 10.3). Instead of waiting for an existing tree to die, they contrive the event. A strangling fig tree begins life as a climber. It wraps itself around an existing tree of another species and grows like a clematis or rambling rose. But, unlike a clematis, the strangling fig's tendrils continue to grow stouter and stronger. It relentlessly tightens its grip on the unfortunate host tree, preventing it growing and eventually achieving the botanical equivalent of throttling it to death. The fig tree has by now grown to a respectable height, and it easily wins the race to the patch of light vacated by the stifled tree. The banyan tree is a kind of strangling fig with an added, remarkable, feature. Having smothered its original host, it sends out aerial roots which, when they hit ground, {307} become proper, absorbing roots but, above ground, serve as additional trunks. So the single tree becomes an entire wood which may be 1,000 feet in diameter and can provide shelter for a medium-sized covered market in India.

  I've been telling fig stories partly to show that the facts about figs are at least as enthralling as anything that my lecturer of Chapter I was able to dig up in mythology or literature, but also to illustrate a scientific way of tackling questions which might serve as a salutary example to that literary dilettante. The facts that I have so briefly recounted are the product of many man-years of meticulous and ingenious work: work that deserves the accolade ‘scientific’, not because it employed elaborate or expensive apparatus but because it was disciplined by a certain attitude of mind. Much of the deciphering of the wasp-pollination story would simply have involved slicing figs open and looking inside. But looking’ gives too laid-back an impression. It wasn't a passive gawping but a carefully planned recording session yielding numbers to be fed into calculations. Don't just pluck figs and slice them. Systematically sample figs from a large number of trees, from particular heights, and at particular seasons of the year. Don't just stare at the wasps wriggling inside: identify them, photograph them, accurately draw them, count them and measure them. Classify them by species, sex, age and location in the fig. Send specimens to museums for identification by detailed comparison with internationally recognized standards. But don't make measurements and counts indiscriminately just for the sake of it. Make them in the service of testing stated hypotheses. And when you look to see if your counts and measurements fit the expectations of your hypothesis, be aware, in calculated detail, how likely it is that your results could have been obtained by chance and mean nothing.

  But let's return to the fig wasps themselves. I said that, in the case of many species of fig wasps, the males in a fig collaborate to dig a hole through which all the females can escape. Why? Why doesn't a male, given that his colleagues are going to make the hole, sit back and leave them to it? Here, in microcosm, is a puzzle that continually intrigues biologists: the puzzle of altruism. An additional problem hampers the biologist seeking to explain the matter to non-specialists. {308} Common sense seldom perceives it as a puzzle at all. So the biologist, before he can get down to extolling the ingenuity of the solution, has to begin by persuading his audience that there ever was a puzzle requiring a special solution in the first place. In the special case of the male fig wasps, the reason it is a puzzle is this. A male that did sit back and let his colleagues make the hole would be able to save up all his energy for mating with females, secure in the knowledge that he need not hold himself back for the effort of making the hole. Other things being equal, genes for refusing to help would spread at the expense of rival genes for cooperating in hole-making. To say that genes for X will spread at the expense of Y is tantamount to saying that Y will disappear from the scene, supplanted by X. Of course, the consequence of this would be that no hole would be dug, and all the males would suffer. But this is not in itself a reason to expect males to dig. It might be a reason if they had human foresight but, assuming that they haven't, natural selection will always favour short-term benefit. Given that all the rest of the males are digging, short-term benefit will be enjoyed by an individual male that
opts out and saves his energy. On this argument, digging should disappear from the population, driven out by natural selection. The fact that this doesn't happen presents us with a puzzle. Fortunately it is a puzzle that we know, in principle, how to solve.

  Part of the solution may lie in kinship: in the high probability that all the males in a given fig are brothers. Brothers tend to share copies of the same genes. A wasp that helps to dig a hole will be releasing not only females with whom he has mated but females with whom his brothers have mated. Copies of the genes that foster cooperative digging will pour out through the hole, riding in the bodies of all these females. That is why those genes persist in the world, and that is a good explanation for the persistence of the behaviour among males.

  But kinship is probably not the whole answer. I shan't spell it out, but there is an element of games playing which has no connection with brotherhood and this applies to the cooperation between wasp and fig. The whole story of wasps and figs is redolent of hard bargaining, of trust and betrayal, of temptation to defect policed by unconscious retaliation. We have already had a taste of this in the {309} Hamilton theory about over-exploited figs dropping to the ground. As so often, I must give a ritual warning that it really is all unconscious. This is superficially obvious for the fig half of the story, since no sane person thinks plants are conscious. Wasps may or may not be, but for the purposes of this chapter we are treating wasp strategy as being on the same footing as the strategy of an indubitably unconscious fig tree.

  The garden inclosed is a paradise cultivated for the benefit of small insects and not surprisingly it is home to a rich and writhing Lilliputian fauna, not just the wasps whose pollination services make it all ultimately possible. Miniaturized beetle, moth and fly larvae abound, as do mites and small worms. There are predators lurking at the very gate of the garden, waiting to cash in on the rich fauna within (Figure 10.4).

  The true pollinators are not the only miniature wasps that live in figs and are lumped under the general name of ‘fig wasps’. There are freeloaders, distant relatives of the bona fide pollinators and parasitic upon them. Instead of entering the fig through the hole at the top, {310}

  Figure 10.4 Perils of being a fig wasp. An ant lurks outside the garden gate waiting for wasps to emerge.

  these parasitic wasps are normally injected as eggs through the fig wall via the spectacularly long and thin hypodermic which is their mother's uniquely specialized ovipositor (Figure 10.5). Deep inside the fig, the tip of the hypodermic seeks out the little flowers in which eggs of true, pollinating fig wasps have been laid. A female parasitic wasp looks and works like a drilling rig, and the hole that she bores through the fig wall is, on her own scale, equivalent to a 100-foot well. Males are often wingless, like the true fig wasp males (Figure 10.6). To crown the story, there are second-order parasites, wasps that lurk by the side of a ‘drilling-rig’ wasp, waiting for her to finish work. As soon as she pulls out, the hyperparasite slips her own, more modest ovipositor into the bore-hole and inserts her own egg.

  Like the pollinating wasps themselves, the individuals of the various freeloading parasite species are playing complicated games of strategy with one another. This was investigated by the same W. D. Hamilton, working in Brazil with his wife Christine. Unlike the pollinators, the freeloader species of wasps often have winged males as well as winged females. Some species have all winged males, some species

  Figure 10.5 Sectioned fig with parasitic wasp females waving their ‘drilling rigs’ in the air. {311}

  Figure 10.6 Freeloaders: parasitic wasps, Apocrypta perplexa, that do no pollinating but benefit from the fig. (a) Female; (b) miniature view of female in ‘drilling rig’ position; (c) male, with no wings and apparently nothing like a wasp.

  have all wingless males and some species have a mixture of winged and wingless males. Wingless males, like the males of pollinator species, never leave their natal fig where they fight, mate and die. Winged males are like females in flying out of their natal fig, where they will mate with any females that have not already mated. So, there are two alternative ways of being a male, and some species exhibit both ways. Interestingly, the rarest species are most likely to be winged and the commonest species most likely to be wingless. This makes sense because a male of a common species is pretty likely to {312} find a female of his own species in the same fig. A male of a rare species, however, is likely to be the only member of his species in his fig. His best hope of finding a mate is to fly away to look for one. Indeed, the Hamiltons found that winged males actually refuse to mate until they have flown out of their natal fig.

  From a strategic point of view we are especially interested in those species that have two kinds of males. It's almost like having a third sex. In fact the winged males look far more like females than they look like wingless males. Both females and winged males are almost believable as wasps, although they are tiny. But the wingless males are nothing like wasps to look at. Many have savage pmcer jaws which make them look a bit like miniature earwigs going backwards. They seem to use these jaws only for fighting — lacerating and slicing to death other males that they encounter as they stalk the length and breadth of the dark, moist, silent garden that is their only world. Professor Hamilton gives us a memorable description.

  Their fighting looks at once vicious and cautious — cowardly would be the word except that, on reflection, this seems unfair in a situation that can only be likened in human terms to a darkened room full of jostling people among whom, or else lurking in cupboards and recesses which open on all sides, are a dozen or so maniacal homicides armed with knives. One bite is easily fatal. One large Idarnes male is capable of biting another in half, but usually a lethal bite is quite a small puncture in the body. Paralysis follows a small injury so regularly and quickly as to suggest use of venom ... If no serious injury results from the first or second reciprocal attempts to bite, one of the males, injured perhaps by loss of a [foot] or in some way sensing himself outmatched, retreats and tries to hide ... From this position he can bite at the legs of the victor or another passing male with much less danger ... One fruiting of a large tree of Ficus probably involves several million deaths due to combat.

  The phenomenon of a species having two distinct kinds of males is not unknown elsewhere among animals, but it is never so pronounced as in the case of the fig freeloader wasps. There are individual red deer stags called hummels which lack antlers yet seem to {313} make a respectable showing of reproducing themselves in competition with their antlered rivals. Theorists have distinguished two possibilities for what is going on in such cases. One is the ‘best of a bad job’ theory. This probably applies to a species of solitary bee called Centris pallida. The two kinds of male bee are called ‘patrollers’ and ‘hoverers’. Patrollers are large. They actively search for females who have not yet hatched out of their underground nurseries, dig down and mate with them underground. Hoverers are small. They don't dig but hover in the air, waiting for the emergence of the few flying females that the patrollers missed underground. Evidence suggests that the patrollers do better than the hoverers but, given that you are a small male with little chance of succeeding as a patroller, you can make the best of a bad job by hovering instead. As always, this is genetic, not conscious, choice.

  The other theory about how two kinds of males can co-exist in a species is the stable balance theory. It seems that this may apply in the case of the fig freeloaders. The idea here is that both kinds of male succeed equally well when they exist in a special, balanced proportion in the population. What keeps the proportion balanced is this. When a male is a member of the rarer type he does well, specifically because he is rare. Therefore more of his kind are born, and they consequently cease to be rare. If they succeed so well that they become common, the other kind now have the advantage by virtue of being relatively rare and they accordingly become commoner again. So the proportion is regulated rather in the manner of a thermostat. I've told the story as if it gave rise to wil
d oscillation but this there need not be, any more than a thermostatically controlled room oscillates wildly in temperature. Nor does the stable equilibrium proportion have to be 50 — 50. Whatever the equilibrium proportion may be, natural selection keeps pushing the population back towards it. The equilibrium proportion is that proportion at which the two types of male do equally well.

  How might something like this work itself out in the case of the fig freeloaders? The first fact we need is that the females of these parasitic species tend to lay only one or two eggs in a fig before moving on to another one (they poke their ovipositor in, you'll remember, {314}

  Figure 10.7 A Garden Inclosed.

  from the outside of the fig). There are good reasons for this. If a female placed all her eggs in one fig, her daughters and (wingless) sons would be likely to mate with each other, and it is well understood that incest is a bad thing, for the same kind of reason as flowers avoid self-pollination. Anyway, it is a fact that the females do spread their progeny around thinly among figs. A consequence is that there will, by luck, be a number of figs that happen not to have any eggs of the species at all. And there'll be a number that happen to have no male eggs and a number that happen to have no female eggs.

  Now think about the possibilities that might face a wingless male wasp. If he hatches out in a fig with no females, there is nothing he can do. That is the end of him, genetically speaking. But if there are any females at all in his fig, he has a good chance of mating with them, albeit in competition with other males of his kind — and it is no wonder these tiny male wasps are among the best armed and most {315} ruthless fighters in the animal kingdom. Few females leave their figs unmated if there are any wingless males inside. Some figs will happen to have female eggs but no male eggs. These females will leave the fig unmated, and the only males that can mate with them are winged males outside.