Masters of Disguise: Animal Mimics Fool Their Foes

The year was 1848. a young British naturalist named Henry Walter Bates had gone to the Amazon with fellow countryman Alfred Russel Wallace to look for evidence of the origin of species. Over the course of his 11-year stay, he noticed that local relatives of a European butterfly known as the cabbage white—the pierids—were bedecked in the showy reds and yellows of rain forest butterflies called heliconids. Observing that the heliconids seemed to possess toxins that made them unpalatable to predators, Bates reasoned that by mimicking the toxic heliconids’ warning colors, the harmless pierids were escaping predation. When Bates returned to England in 1859, the year that Charles Darwin published On the Origin of Species, his discovery of these “mockers,” as he called them, became the first independent evidence to corroborate Darwin’s theory of evolution by natural selection—which holds that organisms best able to meet the challenges in their environment survive to produce the most offspring, so that their traits become increasingly common through the generations.

Apart from Darwin and Bates, though, most biologists were slow to recognize the significance of nature’s impersonators. But now, a century and a half later, mimicry is fast becoming a model system for studying evolution. It is ideally suited to this task because both the selection pressure (predation) and the traits under selection are clear. Indeed, mimicry demonstrates the process of evolution in its most stripped-down form. Discovery of new types of mimicry has also helped fuel fresh interest in the phenomenon among biologists. Joining the classic examples familiar from high school biology class—such as the scarlet kingsnake, whose coloring resembles that of the eastern coral snake, or the viceroy butterfly, whose wing pattern matches the monarch’s—are chemical, acoustic and even behavioral mimics. And stunningly, genetic analyses of one group of mimics have revealed a mechanism by which new species can arise.

Beyond Visual Mimicry
Initially mimicry was regarded as a strictly visual affair, of the kind evident in Bates’s colorful Amazonian butterflies. But it turns out that mimics may fool their foes in other modes. For insects, chemical communication is often more important than the visual variety, and many predators eavesdrop on these chemical conversations for their own ends. The large blue butterfly (Maculinea arion) found across northern Europe and Asia is one notable example. In the 20th century the large blue suffered dramatic declines in many areas and became extinct in Britain in 1979, despite attempts to save it. Agonizingly, that was the very year Jeremy Thomas of the University of Oxford began to realize why conservation efforts had failed: the large blue’s survival depended on the survival of an ant species it mimicked.

In Britain, large blue caterpillars begin life eating thyme plants on warm chalk slopes whose grasses the sheep, rabbits and other grazers keep close-cropped. After the caterpillars molt for the third time, they drop off the thyme plants to the ground, where they launch their false-advertising campaign. The fallen caterpillars emit a chemical signal to attract local ants, tricking them into treating the caterpillars as one of their own. The bamboozled ants carry the caterpillar back to their underground nest, where it proceeds to feast on their larvae for the next 10 months, after which it begins its metamorphosis and eventually emerges aboveground as a butterfly.

Although several species of ants take the caterpillars into their nests, the caterpillars fare well only in the nests of a species of red ant called Myrmica sabuleti. And these ants thrive only when the grass on the chalk slopes is short, allowing enough sunlight in to keep them sufficiently warm. Thomas figured out that as grazing subsided, the grass grew too long for the M. sabuleti ants. As they disappeared, so, too, did the large blue.

Thanks to Thomas’s revelation, scientists were able to reintroduce the butterfly to Britain in the 1980s and help it and the M. sabuleti ants to flourish through careful management of the turf. By 2008, 32 colonies had been established in southwestern England, the largest of which contained 1,000 to 5,000 butterflies per hectare. But one mystery remained: the ants do not just tolerate the caterpillars they bring home; they treat them like royalty, killing their own larvae and feeding them to the caterpillars if food is scarce. In 2009 Thomas determined why. Writing in Science, he reported that in addition to copying the ant’s chemical signal, the caterpillars replicate an acoustic cue. Specifically the caterpillar somehow mimics a tiny noise the queen ant makes, assuring itself a steady food supply. By mastering two key impressions, the large blue tricks the ants into seeing it not just as one of their own but as the most important member of their society.

The large blue butterfly’s subterfuge is not the only instance of acoustic mimicry. This kind of imitation also occurs in one of nature’s classic arms races: the struggle between moths and bats. Bats hunt at night using echolocation, emitting ultrasound clicks and detecting the echoes of these sounds as they bounce off objects in the environment. The result is an aural image of their surroundings—including any tasty moths in the vicinity. This tactic is so efficient that moths have had to develop countermeasures to survive.

Like many day-flying butterflies, some night-flying moths gather toxic chemicals from plants that make them baneful to bats. But whereas a diurnal insect can advertise its toxicity with warning coloration, that strategy would not work for a nocturnal moth trying to avoid a predator hunting in the dark. Tiger moths have evolved especially ingenious solutions to this problem: they emit warning clicks that the bats learn to associate with unpalatable prey. Not all these tiger moth species are actually noxious. But as William Conner of Wake Forest University has found in his experiments, once a bat eats a toxic tiger moth, it will subsequently tend to avoid other sound-producing tiger moths, including perfectly edible ones.

The moths have yet another acoustic trick. In 2009 Conner’s group reported in Science that the more subtly tuned clicks of the edible tiger moth Bertholdia trigona throw the bats’ echolocation mechanism into disarray: the bats attempt to catch the moths but fail. This is true radar jamming, of the kind found in modern fighter planes.

In addition to hoodwinking predators through their coloration, scent or sound, mimics may attempt to con the enemy by assuming the shape of another species. In 1998 biologists working in Indonesia announced the discovery of a small octopus with an arsenal of disguises—Thaumoctopus mimicus, the mimic octopus. Like most octopuses (and their squid and cuttlefish kin), the Indonesian species can change color to blend in with its surroundings. But it was also reputed to do impressions of a menagerie of marine creatures found in the same waters as the octopus—including the lion fish, the banded sea snake and the flounder—not only copying the coloration of these animals but also changing its comportment to mimic their shapes.

So far most of these impressions remain speculative. But in 2008 octopus expert Roger T. Hanlon of the Marine Biological Laboratory in Woods Hole, Mass., reported in the Biological Journal of the Linnean Society that he had found strong evidence that the mimic octopus does indeed impersonate the flounder, holding its tentacles together in a flat, flounderlike shape and swimming in the flounder’s undulating way.

Evidence for Evolution
Mimicry research has, for the most part, focused on the mimetic signal and the way it is received. But for one group of creatures—the Heliconius butterflies that enthralled Bates in the 1850s—we now have a fuller picture: the genetics underlying their dazzling array of mimetic patterns. Armed with this new understanding, scientists have uncovered something that surely would have delighted Darwin no end: a mechanism for the very beginning of speciation, the process by which one population of a species becomes reproductively isolated (unable to mate with other populations) and gives rise to a new species.

The discovery has its roots in research that began about 10 years ago with the work of Chris Jiggins, now at the University of Cambridge, who determined that in addition to being mimetic, Heliconius wing patterns serve another purpose: males use them to identify potential mates. In 2009 Jiggins, working with Mauricio Linares of the University of the Andes in Colombia, described research that illustrates just how dramatic the effects of the interplay between mimicry and mate choice can be. By crossing H. melpomene butterflies with H. cydno ones, Linares managed to breed a hybrid in three generations that exhibited the wing pattern of a wild H. heurippa. In mate choice experiments this hybrid, which had in a sense just evolved, instantly preferred individuals with its own wing pattern to those bearing the different wing patterns of the parent species.

Later that year Marcus Kronforst of Harvard University published a paper in Science advancing that line of research one crucial step further. He demonstrated that the gene for wing color in Heliconius is inherited with the gene for mate choice. That link accounts for the instant preference the artificial hybrid butterflies showed for their doppelgängers. This relation between wing color and mate choice provides a mechanism by which speciation can occur. In a given population of Heliconius butterflies, a mutation leading to a beneficial wing pattern can spread quickly because the mutants prefer to mate with their own kind. Over time two forms that could interbreed but generally choose not to will accumulate other genetic variations that eventually result in the sterility of any offspring produced by their union. Their reproductive isolation complete, two species will exist where once there was one (or in the case of Linares’s butterflies, three species will exist where once there were two).

Working with two populations of H. cydno in Ecuador and Costa Rica, Kronforst has identified the two “ends” of this speciation process. In Ecuador the white and yellow butterflies are two varieties of the same species, H. cydno, separated only by differences in a single gene that flips the wing color from white to yellow. These butterflies appear to be at the very earliest stage of speciation. Their counterparts in Costa Rica, in contrast, have diverged to the point where the yellow form qualifies as a separate species, H. pachinus. Although these two Costa Rican species can still interbreed in captivity, the resulting hybrids exhibit small differences in the wing patterns that render them liable to predation. Presumably genetic differences between these two species will continue to accumulate over time such that they will eventually not be able produce viable offspring at all.

Back in 1863, Bates prophesized that “the study of butterflies—creatures selected as the [exemplars] of airiness and frivolity—instead of being despised, will someday be valued as one of the most important branches of Biological science.” The work of Jiggins and Kronforst and their colleagues has realized that prediction. No doubt the study of other mimics will yield more such insights into the inner workings of evolution.