The Folly of Fools (7 page)

THE COEVOLUTIONARY STRUGGLE BETWEEN DECEIVER AND DECEIVED

The most important general principle is that deceiver and deceived are locked into a coevolutionary struggle. Since the interests of the two are almost always contrary—what one gains by perpetrating a falsehood, the other loses by believing it—a struggle (over evolutionary time) takes place in which genetic improvements on one side favor improvements on the other. One key is that these effects are “frequency dependent”—deception fares well when rare and poorly when frequent. And detection of deception fares well when deception is frequent but not when it is rare. This means that deceiver and deceived are locked into a cyclic relationship, in the sense that neither can drive the other extinct. Over time the relative frequencies of deceiver and deceived oscillate, but they do so within bounds that prevent either from disappearing. Likewise, in a verbal species like our own, we will be warned about new tricks more often by others the more frequent the tricks become. Note that no role is exclusive to some and not others—all of us are both deceiver and deceived, depending on context.

FREQUENCY-DEPENDENT SELECTION IN BUTTERFLIES

You don’t have to look far to find evidence of frequency-dependent selection in systems of deception between prey and their predators. For example, in model/mimic systems, such as are found in butterflies (and snakes), a distasteful or poisonous species (model) evolves bright coloration to warn predators that it is distasteful. This selects for mimics, species that are perfectly tasty and harmless but gain protection by resembling the model. In West Africa, there is a genus of butterfly that is distasteful and as many as five species of the genus, all differing in coloration, may be found in the same forest. It turns out that there is a single species capable of mimicking all five model species. That is, females of the mimetic species can lay five kinds of eggs, each of which grows up to resemble one of the poisonous species.

This unusual system of mimicry provides striking evidence of frequency-dependent selection. Here, one species is delicious but mimics any one of five related poisonous species. These differ in color and pattern, and so do their respective mimics. When several poisonous species are found in the same forest with their mimics, the frequency of each mimic within this species matches the frequency of the model among its group of related, distasteful species. This could have been brought about only by frequency-dependent selection, where each mimetic form loses value when it becomes too common relative to its own model. If all the tasty butterflies looked the same, the predatory birds would rapidly specialize on that one form, decimating it.

One implication of frequency dependency is a perpetual premium on novelty. Indeed, in the above example, novel forms are more common in the mimetic species the more it outnumbers its model. That is, the more frequent the deceivers are, the more they begin to diversify, the better to avoid detection. Every new deception, by definition, starts rare and thereby gains an initial advantage. Only with success will one’s disguise become part of the backdrop against which another novelty can begin rare and flourish. We can also see how easily break-off forms in the mimic might happen to resemble a second poisonous species, leading to two forms mimicking two species.

AN EPIC COEVOLUTIONARY STRUGGLE

A very rich illustration of coevolutionary principles is found in the relationships between brood parasites and their disadvantaged hosts, especially in birds but also in ants. A surprising percentage of all bird species, about 1 percent (usually cuckoos and cowbirds but also including a species of duck), is entirely dependent on other species to raise their young. Naturally this arrangement is rarely to the advantage of the “host” birds, who may end up raising unrelated young in addition to their own—or worse still, as is often the case, unrelated young
instead
of their own. This particular host/parasite relationship has been studied in unusual detail. Indeed, it is mentioned almost as early as human writing permits, some four thousand years ago in India, later described by Aristotle, and recently studied intensively by very clever field experiments designed to tease apart how the relationship works.

The first move is for the deceiver to lay one of its eggs in the victim’s nest. This selects in the victim for the ability to recognize a strange-looking egg and eject it. This, in turn, selects for egg mimicry in the brood parasite—the tendency to produce eggs that have the same spotting and coloration as the eggs of the species whose parental care is being borrowed. Some parasitic species lay in the nests of multiple species, with individual species specialized to lay eggs that match in coloration the eggs of the species in whose nest they are laying. It is now advantageous for the host to be able to count total number of eggs, and reject nests with one too many. This is especially valuable if the parasite’s young hatches before those of the host, ejecting all of its eggs so as to monopolize parental investment, leaving the host no offspring of its own to rear. Better for the host to start over. This selects for parasites that remove one egg for each one laid, leaving total number the same, and the egg is eaten or moved some distance from the nest, perhaps to hide the crime.

Once the egg has safely hatched, selection may favor brood-parasite mouth colors that resemble those of the host species, since parents feed more strongly mouth colors that resemble those of their own species. Within their own brood, evidence from other birds suggests that mouth color may be brighter for healthier chicks, so it is interesting that brood parasites make their mouth colors especially bright. By pushing out its foster siblings, the host young can monopolize parental investment, but since parents adjust their feeding to the total begging calls they hear, a single cuckoo chick may evolve to mimic the calls of an entire brood of the host. In an even more bizarre twist, a species of hawk cuckoo that parasitizes a hole-nesting species in Japan has evolved inner-wing patches that resemble the throat coloration of its host, so that when begging for food, a chick can flap its wings and simulate the begging of three offspring instead of one. The wing patches are even occasionally fed, a case of deception being too convincing for its own good.

A very important selective factor is errors in recognizing a host’s own offspring—so-called false positives—that are an inevitable feature of any system of discrimination (see spam versus anti-spam in Chapter 8). For weak systems of discrimination, a host rarely rejects itself, but it is fooled too often into accepting cowbird chicks. Stronger systems of discrimination cut down on the host’s loss due to the cowbirds but also impose a cost on the host, as it inevitably accidentally rejects its own offspring more of the time. In reed warblers, parents learn the appearance of their own eggs and then reject those differing by a certain amount. If their nests are parasitized about 30 percent of the time, it makes evolutionary sense for them to reject strange eggs, but if they are parasitized less often, the cost in destruction of their own eggs is too great. Sure enough, reed warblers are parasitized only 6 percent of the time in the UK and do not reject new eggs—unless a cuckoo is seen near the nest at about the right time (perhaps pushing probability above 30 percent). In one population, a drop in parasitism rate from 20 percent to 4 percent was matched by a one-third reduction in rejection rate, an effect too rapid to be genetic, so reed warblers probably often adjust their degree of discrimination to evidence of ongoing brood parasitism.

Note the important frequency-dependent effect. When almost all eggs are their own, discrimination will result in the warblers destroying some percent—say, 10 percent of their clutches—with only rare gain. But at 30 percent parasite frequency, they risk harming themselves only 7 percent of the time, while with perfect discrimination, they save themselves a substantial cost (in nurturing other species almost 30 percent of the time). At low frequency, deceivers are hardly worth detecting—only at high frequency are important defenses expected to kick in.

There is one striking peculiarity in the entire system. Birds repeatedly fail to evolve the ability to see that the cuckoo or cowbird chick bears no resemblance to their own chicks beyond mouth color and begging call. In size, a cuckoo chick is often six times or more larger than its host, so that a foster parent may perch on the shoulder of the chick it is about to feed. Since it would seem beneficial to note this absurd size discrepancy and act accordingly, why are birds, in species after species, unable to do so? The answer to the mystery is by no means certain, but there are some interesting possibilities. Failure to make the appropriate discrimination happens preferentially in species in which the brood parasite ejects its foster siblings before they hatch. Thus, if the parent learns the appearance of its own chicks by imprinting on the first ones produced, this will work fine if the first brood is its own, but it will prove fatal if at their first attempt they are parasitized. The host will imprint on the brood parasite and kill its own young whenever it sees them. This will wipe out the host’s entire lifetime reproductive success, since it will now see all of its own chicks as foreign.

More generally, some of the brood parasite’s characteristics are super-optimal from the foster parents’ standpoint. We expect parents often to favor the larger of their chicks as being healthier, stronger, and more likely to provide a good return on investment. This may make foster parents vulnerable to implausibly large chicks that nevertheless release the bias that bigger is better. More to the point, many brood parasites have evolved begging calls that are louder than the host’s and hence presumably harder to resist. Likewise, parasite mouth colors are especially brightly colored. These signals are less costly to magnify than is body size.

There is yet another explanation for hosts’ not discriminating against obvious mimics—fear of the consequences. “Mafia-like” behavior has been described in a couple of bird species, in which a cuckoo or cowbird punishes those hosts who eject their eggs by destroying their entire nest. It becomes a matter of accepting a degree of parasitism or being really badly treated—like a demand payoff (tax) instead of an outright killing. Good evidence from one system shows that accepting the mafia tax leads to greater reproductive success than fighting it—and ending up with a destroyed nest.

Recently it has been shown that there is something resembling cultural transmission of knowledge regarding brood parasites. At least reed warblers can learn from the mobbing behavior of their neighbors toward models of cuckoos (whereas they do not bother to learn from induced mobbing toward innocuous species, such as parrots). Warblers are attracted to the sound of nearby mobbing and approach to observe. If it is a cuckoo being mobbed, they are more likely to approach quickly a model of a cuckoo in their own territory and to mob it. This social learning permits a much more rapid spread of defenses against brood parasites than can occur through genetic change alone. A brood parasite has also evolved to resemble a local hawk, and this resemblance reduces the degree to which it is be mobbed by potential hosts.

Birds are not the only group subject to brood parasites. Ants spend an enormous amount of energy raising large broods that are highly attractive as nurseries to other species. There are as many species of social parasites on ants as there are ant species (about ten thousand of each). Even though the nest may be fiercely defended, parasites have ways of gaining entry, usually by mimicking some part of the ant’s communication system. Caterpillars of one butterfly species manage to get into an ant’s nest by curling up in a ball and emitting the smell of ant larvae. They are then carried into the ant nest, where they imitate the sounds of a queen ant, the very sounds that lead actual queens to be preferentially fed and protected. When food is short, workers will feed young larvae to the pseudo-queens and, when the nest is disturbed, will rescue them over ant larvae. The caterpillars are even sometimes treated as rivals by the real ant queen. This is another example of a deception being too effective for its own good. These kinds of relations have been described for dozens of butterfly species that parasitize ant nests.

In sum, each move is met by a new countermove, resulting in principle in an evolutionary struggle that may last millions and millions of years. This is especially true of relationships between different species, where issues of relatedness no longer apply, but it may be true of many similar relationships within species as well. The two sexes, for example, are partly cooperative and partly in conflict, with move being matched by countermove, locking them into a tight frequency-dependent relationship that usually stabilizes at equal number of the two sexes (see Chapter 5).

Deception can be beautiful, complex, and very amusing. It can also be very, very painful. To be victimized by systematic deception in your own life can cause deep pain. Even watching another species victimized by deception can sear your heart. Every spring in Jamaica, I watch a few dove couples trying to reproduce by raising their young in my trees. These are birds I love to watch, and I wish them every success. Emerge from stage left the anis—large, black, ominous-looking birds that prey on the nestlings of other birds, eagerly gobbling up the chicks. Arriving in groups of about six to twelve, the anis are noisy and fast-moving, saturating their terrain and relying on one heartless trick. One ani gives a loud call that mimics the generic chick begging call of other species—a plaintive kind of squawk that the chick is most likely to give when it is hungry and the parent is nearby. Now the victim chick hears the ani’s begging call and promptly begs itself, the better to outcompete its imaginary sibling. The ani (or one of its group members) makes a beeline to the chick and gobbles it up, along with any other nestlings. Your heart goes out to the victim, fooled by its naive tendency to beg when it hears a begging call. Or worse, you suffer for its silent and completely innocent siblings, only fated to have a fool in their nest. I spent one long evening flinging stones at anis who were about to devour a nest they had detected through this deception. They stayed nearby overnight and consumed the nest contents first thing in the morning.