by Colin Tudge
Enter, though, the Africanized bee. Its aggression is matched by its energy, and it does apparently make the long trek out to the isolated Brazil nut trees. Introduced species on the whole are a bad thing—in fact, “exotics” seem to be the chief cause of extinction of native species, apart, of course, from gross loss of habitat. But here at least, just for once, there is some compensation. “It’s an ill wind,” as the adage has it.
Birds are great pollinators too—notably, but by no means exclusively, hummingbirds. Like butterflies, they typically prefer red, which they see best. Mammals also. Some, like the honey possums in Australia or the desert rats in South Africa, are highly specific. Others, like the capuchin monkeys of Amazonia or giraffes in Africa, may pollinate their prey trees inadvertently (but nonetheless usefully) as they forage. But among the mammals, as with all creatures, the most efficient pollinators are the fliers; and with mammals that means bats.
There are well over eight hundred species of bats—among mammals, only rodents have more species. They are of two main kinds. The microbats live all over the world. Many—like the familiar bats of temperate lands—eat insects; but others live on mammalian blood (the vampires), on frogs, or on nectar and fruit. The megabats, which include the flying foxes, live exclusively in the Old World. For the most part they are big and live largely or exclusively on nectar and/or fruit. They rely heavily on scent to find their food, as most mammals do. By contrast, the microbats locate their prey, whatever it may be, by echolocation: sending out a high-pitched squeak and analyzing the echo. Both groups of bats are nocturnal. If they fly by day—as they sometimes are obliged to do, particularly in cold weather, when there are too few insects flying at night—they are quickly picked off by hawks. Some studies have shown that day-flying bats rarely survive for more than a few hours. Mammals and birds both flourished in the wake of the dinosaurs and flying reptiles. But while the mammals came to dominate the ground, birds very definitely dominate the air. Bats are very successful—ubiquitous and various—but they are advised to stick to the hours of darkness. Even then, they must avoid the owls.
Trees (including many cacti) hold their flowers high for bat pollination.
Trees that would be pollinated by bats must adapt to them—just as they must to specialist bees, butterflies, or moths. None has adapted to them more spectacularly than a relative of the mimosa: the Amazonian tree Parkia. Parkia has been studied in particular by Dr. Helen Hopkins, but it is everybody’s favorite, like a favored sister, endlessly endowed. It is beautifully shaped, like a great flat-topped umbrella. Its leaves are doubly compound, like feathers. Its bark is smooth but not too smooth, in some species dotted with red. But most glorious of all are the flowers, pompoms of stamens and styles, bright red or pale yellow or bronze, depending on species, that hang from on high on long, thin threads like Christmas baubles.
The topmost flowers in each inflorescence are sterile, with copious nectar, which begins to flow early in the morning. By midmorning the first flowers begin to open, and all of them are open by midafternoon. At dusk, the flowers begin to release their pollen. Then the bats come. By morning all the nectar has gone, the filaments that bear the anthers have wilted, and the flowers have faded. One of nature’s most glorious shows lasts only one night. Showbiz is not the point. Replication and multiplication is the point. One night is enough: as we have seen already, animal pollination can be remarkably efficient. The would-be pollinators are constantly alert.
So there are many specific, mutualistic relationships between many different kinds of trees and many different kinds of animal pollinators. But the most stunning relationships of all are between the world’s figs and their pollinating fig wasps. Here we see, writ large, all that is involved: the exquisite precision of coevolution; the sacrifice that the figs must make to entice the wasps; the constant temptation on both sides to renege; and the inevitable imposition of freeloaders (including parasites).
OF FIGS AND WASPS
All organisms are different, but some, as George Orwell might have said, are more different than others. There is nothing quite like an octopus. There is nothing quite like a human being. And there is nothing, absolutely nothing, like a fig. Figs, as described earlier, are of two main kinds: the kind that grow as other trees do, when planted in the ground, and the kind that begin as epiphytes. The epiphytes in turn may be stranglers, encircling and throttling their hosts, or nonstranglers that, like banyans, begin aloft but contrive to make contact with the ground without crushing their hosts. (In the Solomon Islands, too, a few kinds of figs grow as climbers.) In all kinds, the young fruits take the form of “syconia” (not “synconia” as often printed). They are like fleshy cups, though almost closed at the top. The flowers, often hundreds of them, are borne inside the cups, facing inward. The effect is womb-like, as D. H. Lawrence was not slow to observe. Each female flower contains only one ovule, which, when the flower is pollinated, develops into a seed. If the flowers are not pollinated, then the entire fruit aborts—or that, at least, is what usually happens; for as we will see, there are twists. (Strictly speaking, a syconium does not become a fruit until the seeds are fertilized. But it is convenient to use the term “fruit” to mean syconium.)
The syconium (fruit) of a fig is both womb and sepulchre.
The flowers inside their syconia are pollinated by small black fig wasps. A female fig wasp enters the syconium through the hole at the top and lays her eggs in some (up to half) of the flowers. A wasp that colonizes a fruit establishes a new generation of wasps; and so she is called a “foundress.” After she has laid her eggs, she dies. The fruit becomes her sepulchre. Each egg hatches into a larva, which feeds on the developing seed within its allotted flower (which, of course, kills the seed). Then the larvae pupate, each one still in its flower, until they emerge as adults. At least half, and often more than 95 percent, of those new young wasps will be females; less than half, and often fewer than 5 percent, will be male. The males are wingless. They emerge before the females, chewing their way out of their respective seeds. Then they chew their way into seeds containing females and mate with them while the females are still inside. After mating, they, too, die. The newly emerged females, already with sperm on board, now fossick around inside the syconium, picking up pollen from the male flowers, although they do not apparently feed on it. Then they fly off to found a new generation in a new syconium. These young females are laden with pollen, and so they fertilize the flowers of the next syconium.
The net result is a wonderful mutualism. The figs benefit, because they get their flowers pollinated, and so are able to set seed. The wasps benefit, because they are supplied with a good, safe place to lay their eggs and a food supply for their larvae. Without the wasps, the figs could not reproduce, and so would die out; and without the figs, the wasps could neither reproduce nor feed. Although the wasps are small they fly prodigious distances, so any one fig tree may spread its pollen over thirty-nine square miles. Indeed, in the gallery forests of Africa it seems that individual wasps may carry the pollen from some trees hundreds of miles: presumably the wasp rises into the upper air currents and is whisked along (though how it knows when to descend again, and how it does so, is not at all obvious). This has been discovered not by studying wasps directly but by DNA studies of the figs, which reveal that any one fig may have daughters living a very long way away.
Figs are immensely successful. More than 750 species are known—more even than for oaks or eucalypts—and they thrive throughout the tropics, both Old World and New, and into the subtropics. Extraordinarily—indeed, it all starts to seem miraculous —each kind of fig has its own species of symbiotic wasp. Each wasp coevolved with the fig it pollinates.
This, at least, is the basic story. It was beginning to unfold even by the 1940s, and has been steadily expanded since by generations of biologists. The research has been outstanding. It is difficult to do, but figs are of tremendous ecological importance—the sole or the standby food supply for hosts of forest
creatures; and the study of mutualisms, as Darwin himself first noted, is a rich source of evolutionary hypotheses that also offers the means to test them. Modern techniques, including molecular methods that enable researchers to explore the evolutionary and genetic relationships between different figs and different wasps, are enriching the insights month by month. The following account is based mainly on the extraordinary studies over the past two decades by Dr. Edward Allen Herre and his colleagues at the Smithsonian Tropical Research Institute (STRI) in Panama (which I was privileged to visit in 2003).
To begin at the chronological beginning: how did the precise relationship between fig wasps and figs—basically one fig per wasp, with hundreds of species of each—first evolve? It is impossible to reconstruct history with certainty, but modern investigations are providing many intriguing insights.
First, genetic and anatomical studies show that all the wasps that pollinate figs are descended from a common ancestor. Comparable studies suggest that all modern figs are also descended from a common ancestor. The two facts together imply that the present-day mutualism of figs and their pollinating wasps evolved only once. All the 750 or so species of figs and their corresponding wasps are descended from one kind of fig and one kind of wasp that first appeared a very long time ago. Furthermore, as each lineage of figs divided to form two daughter species, so the wasps that pollinated them also divided into two new species: a new kind of wasp for every new kind of fig.
The differences observed in the DNA of existing fig wasps suggest that they last shared a common ancestor around ninety million years ago. The same is true for existing figs. So that, presumably, is when the ancestor of today’s fig wasps (who presumably up to then had been making a living in some other way) began to lay its eggs in the developing seeds of the figs’ first ancestor. Ninety million years ago was when the last wave of dinosaurs and the great marine and flying reptiles were still in their prime.
So figs and wasps have depended on each other, and have coevolved in step—each new kind of fig accompanied by a corresponding new kind of wasp—for tens of millions of years. Clearly the partnership works very well: both figs and wasps benefit. Clearly (we might suppose) it is in the interests of both fig and wasp to keep the alliance intact. Thus biologists traditionally argued that in such relationships as this, natural selection must favor true and stable mutualism. Peaceable, not to say amiable, mutualism has often been portrayed as the natural end state that would inevitably come about sooner or later. But modern theory suggests that it could be in the short-term interests of either party to cheat; and since natural selection does not look ahead, we might expect that short-term betrayal would indeed take place. Modern studies by Dr. Herre’s group and others elsewhere now show that in reality the relationship between figs and wasps has often been reneged upon and otherwise flouted, in various ways and to varying degrees. So biologists must now ask how it is that wasp and fig have served each other so well for so long even though it would pay the wasps to cheat (and the figs too, although probably to a lesser extent).
The relationship between the two can be analyzed in the vocabulary of game theory or, indeed, of cost-benefit analysis. The bottom line is that the figs and the wasps must each pay a price for the services of the other, but neither can afford to pay too much. The figs sacrifice a lot of their would-be seeds—up to half of the possible seeds in each syconium feed the young wasp larvae. The wasps, on the other hand, seem to exercise restraint—for if they lay their eggs in half the seeds, then why not in all of them? To be sure, this would kill off the figs, the geese that lay the golden eggs. But such things happen in nature—precisely because natural selection does not look ahead, and the long term is sacrificed to the here and now. Alliances of wild creatures are known to break down sometimes, and have led to mutual extinction. In the same way, human societies have often broken down as agreements are reneged upon, to the short-term advantage of some but sometimes to the total destruction of all. Why, then—since it would apparently pay them to cheat—do the wasps exercise restraint?
Just to stir the pot a little more: wasps benefit figs by dispersing their pollen—and as we have seen, the active pollinators are especially adapted to do so. But why? What’s in it for the wasp? In the long term they benefit, of course—fertilizing seeds provides a future generation of figs. But since natural selection cannot consider the long term, we always have to ask, what is or was the short-term advantage in any particular mode of behavior? In this case, why does it benefit a pollinating wasp to play an honest game?
In truth, the fig could well have evolved mechanisms to prevent cheating. Perhaps the seeds in any one syconium are not all edible. Plants are remarkable chemists; and virtually all organisms are capable of some degree of polymorphism—producing some offspring of one kind, some of another. Figs could well produce some would-be seeds in a tasty form, to serve as sacrificial offerings to the essential wasps, and others that the wasps find foul and leave alone. There is some preliminary evidence to suggest that something like this is happening, but the picture is not yet clear.
But why (in the short term) should the wasps—the active pollinators, in particular—go to such lengths to pollinate the fruits they invade? Why not simply pinch the ovules in the syconia they colonize without bothering to fertilize the ones they leave alone? The answer seems to be that any syconia whose ovules remain unfertilized are aborted. No pollination, no nourishment. There is, as the adage has it, no such thing as a free lunch. In short, the fig seems to have rigged the game so that the wasp does gain short-term benefit from playing honestly, and would be punished even in the short term if it cheated.
Such mechanisms seem to have kept the whole system on course. Yet (so the Smithsonian studies have shown) it clearly is not quite so stable as has been supposed. Thus it looked for a long time as if the simplest rule applies: each species of fig has its own particular species of wasp; each wasp is adapted to only one kind of fig. But modern techniques enable biologists to explore the relationships between different creatures by examining their DNA. DNA really is a most obliging molecule. Some bits of it—notably some apparently nonfunctional bits known as “microsatellites”—change so rapidly that differences between them reveal relationships even within families: who is whose sibling, or parent, or offspring. (These are the kinds of studies used in legal paternity cases.) Other bits of DNA change more slowly, and significant differences between these bits indicate that different individuals belong to different species. This, of course, is especially useful when two or more different species look very similar. Thus DNA studies in recent years have revealed that various populations of owls, mice, monkeys, and bats that were each thought to represent just one species sometimes should be divided into two or more. When species can’t be told apart except by their DNA they are called “cryptic” species.
By DNA studies, the Smithsonian biologists have shown that fig wasps include many cryptic species. They even found cryptic species within the ancient wasp genus Tetrapus—suggesting that rule that says “one fig, one wasp” has long been “routinely violated,” as Allen Herre puts the matter. We might reasonably guess that when two species of wasps pollinate the same kind of fig, this is simply because some ancestral species of wasp, which served that particular fig, had split to form two species. But DNA studies show that sometimes two different kinds of wasp sharing one fig are not close relatives. This means that one of the two must have come from some other kind of fig. As seems to follow, it also turns out that some kinds of wasps colonize more than one kind of fig. So fig wasps can be more like honeybees than had been supposed. When two kinds of wasps meet in one kind of fig, they might in theory hybridize—and DNA studies show that this sometimes happens; although the hybrids do not themselves seem to spread. When one kind of wasp pollinates more than one kind of fig, the figs could be hybridized—and as we have already seen in willows, hawthorns, poplars, and many others, including the London plane, hybrid plants of all kinds can and do evolve into
new species (and perhaps this is one reason why there are now so many different species of figs).
In the Smithsonian’s Panama studies, when more than one kind of wasp colonizes the same syconia, both wasps may serve as perfectly good pollinators. But this is not always so. A study in Africa has shown that at least in one case, one of the cryptic wasps that colonizes one particular species of fig tree behaves simply as a parasite. It lays its eggs in the flowers and so feeds its young, but it does no pollinating. It is a cheat: an archetypal freeloader. Game theory predicts that freeloader fig wasps might exist—it’s a possible niche—and so they do. Again we see that the simple one-to-one relationship between figs and wasps, evolved over millions of years into perfect mutualism, is not quite so cozy as it has seemed. The relationship, like all mutualisms, is dynamic. It is always prone to decay.
Often, too, any given fruit may be colonized by more than one foundress from the same species. This raises another set of complications—complications that again have been predicted by modern evolutionary theory, and that again (very satisfyingly) have now turned out to be what actually happens.
Let me refer you back (as Perry Mason would say) to an earlier comment: that the proportion of young male wasps born within a given syconium varies from around 5 percent (one in twenty) to around 50 percent. The preliminary point is that many creatures can adjust the sex ratio of their offspring. Humans cannot do this, but we do not shine at everything. Such adjustment is especially easy for wasps (and bees and ants) because in these insects, the females all develop from fertilized eggs, while the males develop parthenogenetically, from unfertilized eggs. The mother wasp (or bee or ant) keeps the sperm separate from her eggs until the time comes for laying, so she can decide in the light of circumstance whether or not to fertilize them before laying. Again the mechanism seems so subtle that it beggars belief, and yet it is the case.
