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  Each Ant, Teach Ant

  WE—AND other animals—can learn things from objects in the world around us, like Dyer's bees or the wasps that remember the location of a rock near their nest. But most of us remember learning in school, from teachers. Insects may lack classrooms and textbooks, but increasing evidence suggests that they too can learn from, and act as, teachers.

  In common use, the word teaching usually means the transfer of information from one individual to another. A boy sees his sister feed the dog under the table and promptly learns to get rid of his unwanted broccoli the same way. Under that definition, though, even casual observation of another animal doing something that the observer then does would qualify. You could learn to run away from fires by noting a crowd fleeing a burning building, for instance, but has the crowd actually taught you? Even Charles Darwin suggested that many animals, including insects, do this; bees, he pointed out, could follow another worker flying to a source of nectar. If crickets are placed in a container with other crickets that have been hiding under leaves from predatory spiders, they are more likely to find a shelter and hide themselves. But this kind of use of public information seems a bit too haphazard to be real teaching. Animal psychologists are more stringent in their definition and often require the behavior to happen only when a naive observer (one that doesn't know how to do the task being taught) is present. That means that although a young male white-crowned sparrow learns his song from his father, the father isn't teaching him, because the adult bird would sing whether or not his son were there. Teaching also has to help the observer while costing the teacher something, usually the time and effort required for the demonstration.

  Finding an occurrence of this more narrowly defined behavior in nature has been daunting, and until very recently scientists had essentially no examples of real teaching by animals. Just within the last few years, however, researchers have found three cases of it—one in a bird, one in a mammal (the meerkat), and one, in credibly, in ants. People are often surprised by the selectivity of this group, suggesting that surely some other primate besides humans teaches in a natural setting. At least for the moment, the answer appears to be no, which says something about our anthropocentric desire to only see, or bestow, special qualities on those we think are closest to us. That teaching happens in ants and not monkeys or apes is unsettling for the same reason I love studying insects: it's all about getting to the same destination with different modes of transportation.

  As anyone who has had to battle the brown ribbons of workers heading toward the sugar bowl knows, ants follow each other to get to food sources. It looks like they are just marching endlessly, one after the other, perhaps following the smell left behind by earlier foragers, but paying no more attention to each other than riders on the same subway train. Odor does play an important role in leading ants to food. But in at least one ant species, a single worker will actively recruit another ant to follow her to a food source or a new nest, or just to explore a new area, in a process called tandem running. The lead ant goes in front, while the follower keeps contact by tapping her with her antennae. If the follower gets behind, the leader waits for her to catch up, and spends time on the task that wouldn't be needed if the leader were alone, fulfilling the criteria outlined above. According to Ellouise Leadbeater and her Queen Mary University of London colleagues, who didn't do the research but study similar kinds of insect social behavior, "The intimate interaction between leader and follower in a pair of tandemly running ants at first sight bears all the hallmarks of a parent teaching a child to ride a bicycle." After being led, the following ant is able to find the target on her own, showing that she has indeed learned from the leader.

  This is big news. As an accomplishment it may not rank with conveying the beauty of Shakespeare to a high school senior, but it means that even ants can respond to feedback from other individuals and modify their behavior so that they improve their performance. Feedback makes teaching different from so-called telling, where in effect one individual says, "Hey, there's a puddle of jam over in the north corner of the countertop, see you there," and then just takes off for the food. This behavior has therefore made scientists question how they define learning, teaching, and their prerequisites. Some researchers feel that because the ants don't improve the skills of those they teach, but simply lead their students along a path, the behavior doesn't really constitute teaching. But in a paper with the subtitle "Ants Are Sensitive Teachers," Thomas Richardson, who led the original project on tandem running, and his colleagues at the University of Bristol in the United Kingdom muse that the arguments over whether the ants are "really" teaching may just be "tracking our own understanding of what is special when humans teach.... We should thereby avoid succumbing to the understandable temptation to use the most exotic, extreme case, i.e., the human one, to define what is perhaps a relatively common phenomenon." In other words, once we find that ants do something like teaching, we should not redefine teaching so only humans can be said to do it. And if ants do teach, what other animals might be showing the same thing, if we only open our minds to see it?

  Smarter Is as Smarter Does

  THE GENIUS of ants notwithstanding, if the basic components of learning and even intelligence lie within a great many creatures, why then are our minds so different? Why do we talk about crows and raccoons and dolphins being intelligent, but chickens and cows as dumb? Is being smarter always better? And if it is, why haven't all animals evolved to be smarter?

  The answers to these questions come from an unlikely source: the humble fruit fly. Now, I can usually sell people on crickets, and ladybugs, ants, and bees already get their own movies, toys, and children's songs. People are less than enthusiastic, though, about the possibility of a sparkling intellect lurking in the sesame seed-sized flies that buzz in clouds around decaying fruit. But in Tad Kawecki's laboratory at the University of Fribourg in Switzerland, fruit flies are contestants in an unending game of Jeopardy, insect style. And some of them are big winners.

  The flies don't learn How the West Was Won or Celebrity Children, but they do have to master a category that might be called Distinctive Odors, by deciding whether to feed and then lay their eggs on a substance that smells like orange or one that smells like pineapple. One of the two offerings is infused with quinine, which tastes bitter, and the flies avoid that odor and fly over to the other area. Once the quinine is removed, some of the flies still remember to stay away from the place that had the nasty taste, showing they have truly learned the association. Then Kawecki takes the eggs that were laid in the tasty stuff, rears the adults that emerge, and repeats the whole experiment again and again. This means that only the genes from the flies that performed the discrimination correctly are passed on to the next generation. It's the same principle—artificial selection—that farmers have used for centuries to generate cows that give a lot of milk or corn that has large ears, but much faster and with an end product of faster-learning flies rather than county fair material.

  Doing these experiments requires painstaking maintenance of the tiny flies in hundreds of jars held under exactly identical conditions—the same temperature, the same food, and in complete darkness. Most modern biology buildings have elaborate facilities for keeping the insects, but of course many scientists labor in less-than-ideal circumstances. As it happened, Kawecki used to work at the University of Basel, also in Switzerland, where his lab was in a crumbling fifteenth-century building in which the doctoral students used a former lecture hall of Friedrich Nietzsche for their office. Although charmingly located on the banks of the Rhine River and architecturally impressive, the building suffered from a variety of maintenance ills, many of which required the service people to enter the attic. The attic in turn was occupied by numerous pigeons and swifts, and one of the building maintenance workers complained so vociferously about the birds' lice and fleas he supposedly encountered in his effort to repair things that an exterminator was called in. While most people welcome the removal of inse
cts from their homes, in a building where precious experimental flies are being kept, the situation is somewhat different. Kawecki and his colleagues made numerous panicky phone calls to the exterminators to make sure the process wouldn't decimate their subjects, and were assured that all would be well.

  Unfortunately, as Kawecki puts it, "the only animals [the exterminator] knew about were cats and budgerigars," and the insecticide proved fatal to some of the carefully reared fruit flies. Luckily, the scientists had to stagger the breeding of the flies because they didn't have enough room to raise them all at once, so they did not lose all of their years of effort. But Kawecki remains nettled at the company, which never admitted any wrongdoing, instead suggesting "it was our fault, keeping those stupid flies rather than cats and budgerigars, as proper Swiss citizens do."

  Despite these setbacks, one generation of flies led to another. Through the selective breeding process, the flies rapidly improved their ability to remember which substance was attractive and which was not, and after about twenty generations, Kawecki had flies that could go to the bug equivalent of Harvard or Princeton. Instead of taking three hours to learn which substance has quinine in it, the new and improved flies knocked the task out in less than an hour. What's more, they could generalize their ability to other tasks that required them to avoid or prefer one odor to another, and even to other stimuli besides odor, which means that the flies were not simply evolving better discrimination of pineapple versus orange, they were actually getting smarter.

  Presumably, being able to detect good places to feed and lay eggs faster would also be useful in the real world, outside Kawecki's lab. So why don't flies show this brainiac capacity naturally? To put it another way, if the flies can get to be so smart, why aren't they rich, or at least more successful?

  The answer seems to be that they don't live long enough. The life span of flies from the smarter lines averaged 15 percent shorter than their unselected relatives. Furthermore, the smarter females laid fewer eggs, an ominous characteristic from the standpoint of evolution, since it means fewer potential copies of genes in future generations. The decreased survival was particularly notable when food was in short supply, which gives a clue to the reason for the finding: learning is costly, and investing brain resources into intelligence may mean that you pay the price somewhere else. More brain, fewer eggs. The trade-off even occurs within the lifetime of a single fly. A group of flies that was trained to associate an odor with a mechanical shock and then deprived of food and water died 4 hours earlier than flies that were exposed to the smell or the shock but didn't have to go through the training, suggesting that something about the process of remembering the association drained the resources of the diligent flies.

  Such trade-offs are common among living things, as I discuss in the chapter on personality. Animals that have many young also tend to have smaller babies, whereas species like us that give birth to one or a few offspring at a time generally produce relatively large ones. Here the trade-off seems to be that when natural selection gives a good learner, it takes away a long life. This could happen at two time scales. Within the lifetime of the fly, the energy a fly acquires could go either to helping it survive longer, or to nervous system machinery, but not both. It may be cheap to upgrade the memory in your laptop, but doing so in the brain is going to cost you.

  Over many generations, a different process may be at work. Say that a gene makes a fly smart, but because most genes have more than one effect, it also makes the fly vulnerable to starvation, or maybe more susceptible to infections. If being smart is advantageous enough—in Kawecki's lab, it made the difference between reproducing or not—then the gene conferring it will persist in the population, even if it also has some downsides.

  Of course, it's not as if all animals get to go to some primordial retail smorgasbord and shop for a certain number of abilities, with some picking learning, long legs, and a mean tennis serve, while others choose curly eyelashes and a talent for languages but end up dimwitted. Exactly which abilities end up having to trade off against which others is still a mystery. But Kawecki's work suggests that the ability to learn, and hence perhaps intelligence, exacts a high price. And that in turn could shed some light on our own evolution. Humans may well have given up some other abilities when we evolved our large brains. What's more, having to learn everything from infancy, rather than being born with our skills, makes our childhoods vulnerable to everything from hot stoves to saber-toothed tigers or their modern-day equivalents. The trade-off in our case must have been substantial, but scientists are still wondering about exactly what it was that we humans had to pay for our intellect.

  Better Learning through Chemistry

  ONE OF the wonderful things about using animals such as fruit flies and other insects to study learning is that they present a window into the brain. Exactly what happens in the body when you learn the capital of Mongolia, or how to get to the theater? We all have some vague idea that nerve cells send messages somewhere, that electrical impulses in the brain do ... something. And we can use complicated brain scans with colorful images of different centers of nerve activity, or detailed dissections, to try and figure out what that might be. But insects, unlike humans, let us alter a chemical here, or breed up offspring with a special mutation there, which means it is sometimes possible to pinpoint precisely what makes an individual able to perform a certain task. If one bug has gene variant A, and another bug's genes are exactly like it except for having gene variant B, and if the two differ in the time it takes them to find a food reward in a maze, then presto, we have a gene linked to learning.

  In most cases, those carefully bred and engineered insects are fruit flies. In the chapter on personality I mention the "rover" and "sitter" flies, which exhibit genetically programmed differences in behavior. Kawecki and his colleagues, most notably Frederic Mery, examined these tendencies in light of their studies on learning. Each behavior is associated with a form of a single gene, and flies with the rover variant of the rover-sitter gene have better short-term, but worse long-term memory, something of a reversed Alzheimer's, where it is easier for sufferers to recall events of decades past than what they had for lunch. Sitters show the opposite pattern and can remember associations from several days ago, but not the fly equivalent of what they ate at an earlier meal. These different strengths and weaknesses make sense in the natural world of a fly; rovers are likely to move from one food source to another, so being able to quickly learn whether a given fruit is ripe or not is more important than remembering what happened in the more distant past. Together with Marla Sokolowski from the University of Toronto, who first discovered the rover-sitter dichotomy and has worked on its details for many years, the scientists then discovered that the differences in memory can be manipulated by increasing or decreasing the amount of an enzyme in the odor detection centers of the insects' brains. That enzyme may be the key to the trade-off between memory types, at least in flies, and suggests some interesting directions for similar studies in people.

  Another set of experiments focused on a different chemical. Using a modified version of the Tennessee Williams paradigm, in which flies are placed into a chamber that heats up on one side when the flies move to it, a group of researchers from the University of Missouri recently demonstrated that serotonin, the same brain chemical that features so prominently in human depression and its treatment, is key to the tiny flies being able to learn to avoid the hot spots.

  The ability to stick to a task after having been distracted—something many children with learning disabilities struggle to accomplish—is also controlled by a few nerve cells and chemicals. Flies tend to move toward a visual object, for example, a stripe on the end of their container. If you remove the goal and show them a "distracter" stripe somewhere else, they veer off for a short time but can still remember where the original stripe was located. Geneticists have bred flies with mutations in various genes that produce chemicals important in learning (as with many specialized strains
of fruit flies, these have fanciful names such as dunce and ignorant), and it turns out that while some of the mutants can still perform the task of recalling their goal as well as normal flies, others cannot. The mutant amnesiac, for example, learns just fine in the first place, but forgets what it learned almost immediately. This distressing tendency can be attributed to a defect in a single neurochemical, one that is extremely similar to a chemical in the human nervous system. Being able to break down a behavior such as recovering after a distraction into components so fine that we can determine exactly which gene is responsible for which part of learning is possible only in insects, at least so far, but maybe someday we will be able to extend this kind of detailed understanding to our own learning difficulties. What's more, the prospect of altering or curing defects in memory with gene therapy in insects suggests that similar treatments may eventually substitute for drugs or surgery in humans, a solution that could have fewer side effects and be targeted more precisely than current approaches.

  He Who Learns Last

  WHICH came first, learning or instinct? Because humans rely so heavily on learning, we tend to think of it as an innovation, an evolutionary novelty that we alone have mastered. In effect, we like to think we invented invention. But centuries ago, naturalists believed that instincts, behaviors that are performed more or less the same way every time, arose after learning. Early animals, they claimed, had to learn things from scratch, and then after time, the repetition of a task was somehow impressed into the fiber of the organism so that eventually it became instinctive. This idea was particularly championed by Jean-Baptiste Lamarck, the French biologist whose ideas about the inheritance of acquired characteristics were first embraced by early evolutionists, including Charles Darwin, but later discredited. Knowing nothing about how genes and chromosomes could be passed from parents to offspring, Lamarck and his contemporaries reasoned that if, say, a horselike animal continually reached for its food at the top of a tree, its neck would become longer. This greater development would then somehow be passed onto its offspring, who in turn would develop even longer necks, eventually resulting in what we now call a giraffe.