Sex on Six Legs Read online

  Paper wasps do not show the extreme differences among castes seen in ants or honeybees, but the scientists were able to examine DNA from four kinds of individuals. Foundresses are the females that start up a colony in the spring, usually by themselves, which means they forage as well as reproduce. They rear the first generation of daughters, who then become workers, allowing the foundress to become a queen and spend all of her time laying eggs. Finally, gynes are females that mate late in the year, spend the winter in a sheltered place, and then emerge in the spring to become foundresses.

  Despite the identical outward appearance of the four types, and the fact that in some cases they are actually the same individuals performing different tasks, the researchers found that the wasp females differed markedly in the expression of genes in their brains. Workers had brains that were more like the foundresses that also cared for young than the queens and gynes that reproduce. Some of the genes that differed in expression were related to the production of insulin, an important component of nutrient regulation in insects, as in humans, which suggests that becoming social involved evolutionary changes in how food is perceived and processed. Toth and Robinson believe that the path from completely solitary to intensely social made use of a kind of molecular toolkit common to the ancestors of both kinds of behavior, modified in small ways as natural selection acted on the components. This differs from earlier ideas that new behaviors needed new genes.

  The Collaborative Dictator

  RESULTS such as these are leading us to a much better understanding of what it means to have genes control anything, whether that is social behavior or eye color. People often assume the existence of a gene "for" a trait, so that if you have the monogamy gene, for example, you won't cheat on your spouse, but if you lack it, your infidelity is inevitable. Studying genomes shows this is futile. First, genetic material is often redundant, nonfunctional, or just plain disassociated from any obviously useful protein. Second, genes are the great recyclers—all of our genes were modified from preexisting ones, with some new mutations that occurred at random thrown in. The genes associated with parental behavior are related to those that make a bee more likely to feed her sister, which are also associated with myriad other behaviors. This means that no gene can be associated de novo with a single trait and that trait only. Third, and maybe most important, genes are regulated with a complexity that is only just beginning to be understood. As in the paper wasps, it's not the genes themselves that change, it's the conditions under which they are expressed, and that regulation requires a host of other genes.

  This is not to suggest that we shouldn't try to explore the genetic basis for behaviors such as courtship or maternal care. On the contrary, the new technologically sophisticated methods can reveal extraordinary detail about the mechanisms behind even complicated behaviors. But we should abandon, once and for all, the antiquated notion that we will ever have a catalogue of genes that can be neatly assigned to one and only one characteristic, that a gene associated with long eyelashes will have no truck with one making us more likely to prefer salty foods. Genes may dictate the production of proteins, but they do so in a maze of collaboration with other bits and particles of DNA.

  What Next?

  GENOME sequencing seems to induce a kind of greed in scientists, a hankering for more species with more variants of behavior and appearance. Many biologists have a favorite study organism and so often would love to have "their" animal or plant sequenced next. As the costs of processing samples decreases, the need to set priorities won't be quite so pressing, but right now several scientists have come up with justifications for "wish lists" to help guide future efforts.

  Evans and Gundersen-Rindal used four criteria to evaluate groups of insects for their place on the list. First was genome size: smaller genomes are easier to sequence, and we already have an idea of genome size for many of the major categories. As mentioned earlier, flies, butterflies, and the bees and ants all have relatively small genomes, while grasshoppers and crickets, cockroaches, and silverfish, those odd little wingless pests in libraries, all have rather large ones. The central database called GenBank already has information on proteins in some of the groups, particularly flies, which also helps in starting a sequencing project. Evans and Gundersen-Rindal also ranked the insects for species diversity within each group, arguing that we would be better off working with diverse groups because they are likely to have more researchers working on them. Finally, they scored the insects for their effect on humans, where, as you might imagine, the elusive silverfish were pretty low on the scale. Overall, they plumped for more flies, more social insects such as bees and ants, and more beetles, with some moths and butterflies thrown in as well.

  Beetles, particularly dung beetles, were also favorites of biologists Ronald Jenner and Matthew Wills, who suggested that the horned dung beetles in the genus Onthophagus would be particularly useful. As with antlers on deer and moose, the horns are more developed on males and are used in fights between rivals for females, allowing researchers to examine the genetic control of sexual differences. What's more, horn size is influenced by the environment in which a beetle matures, with better nourishment yielding more impressive weaponry; this could yield insights into the ways that genes are switched on and off by external factors.

  Using criteria roughly similar to those of Evans and Gundersen-Rindal, myrmecologist and insect photographer Alex Wild mused about which ants would make the best candidates for genome projects. He settled on seven prospects, including the leafcutter ants of the New World tropics, which as their name implies slice off bits of vegetation that they bear off to the nest, where the material is chewed and used as a base for fungus gardens. The wood ants were another favorite, with many examples of social parasitism, potentially giving insight into the evolution of this unusual life history. One of the responses to Wild concurred with his proposal of another species, the bullet ant, which has an exceptionally painful sting, although the enthusiasm seemed to stem more from a desire for revenge by a victim than any biological justification.

  The future clearly contains no shortage of animals to examine. I have a sneaking interest in those silverfish, though. Turns out they have some pretty bizarre mating tactics; the male spins a thread between a vertical object, such as a twig, and the ground and places a sperm packet beneath the thread. He then coaxes a female to walk under the silk, where she picks up the packet with her genital opening. After the sperm have drained into her body, she detaches the packet and eats it. The genetic story behind this kind of sex at a distance must be pretty amazing.

  Chapter 3

  The Inner Lives of Wasps

  Personality in Insects

  IN The Sword in the Stone, T. H. White describes how the magician Merlin educates young King Arthur by turning the boy into various beasts: a fish, a snake, a badger. He transforms young Wart, as he is called, into an insect only once, and that only because Wart is confined to his bedroom, with Merlin shouting at him through the door, and more substantial spells have a hard time entering the keyhole. (The logic of this constraint has puzzled me ever since I first read the story as a child, given Merlin's other superior abilities, but perhaps White felt it necessary to find some justification for why one would ever become an insect in the first place.) In any event, Wart becomes an ant, and it is not a happy transformation. Instead of being thrilled at, say, his ability to lift objects heavier than he is, or his exquisite sense of smell, or his remarkable ability to walk on vertical surfaces, the ant-boy is horrified by the lack of individuality among his nest mates. Each ant (with its "mute, menacing helmet of a face") is like every other, obeying the rules of the queen without questions, and a sign above the tunnel states, "Everything not forbidden is compulsory," a slogan that Wart "read with dislike, though he did not understand its meaning."

  Although the ants turn out to have many unpleasant qualities, the most chilling one is that they are automatons, with no independent thoughts, designated only by numbers and lett
ers and interchangeable in their repetitive tasks of collecting food and burying their dead. This image of insects, particularly the social species such as ants and bees, is behind countless dystopian views of the behavior of extraterrestrials in science fiction, perhaps best personified, if that is the correct term, by the Borg of Star Trek. These cyborgs assimilate all other beings that cross their path, intoning, "Resistance is futile." They have a queen, work unceasingly, and most crucially, like the ants in White's book, lack all individual identity, having sacrificed it for the good of the group.

  Nothing is more important to us than our uniqueness as individuals, and we point to our different personalities as evidence of our humanity. Conformity within the tribe may be valued differently across cultures, but no one thinks a society in which personality is subsumed by service to the state is desirable, even the most diehard communist. Individuality is something of an excuse for selfishness. And while we may freely admit to our pets being distinct individuals, or be willing to believe that a particular elephant or gorilla might be brave or shy, confident or anxious, the buck stops firmly at the backbone. Invertebrates in general, and insects in particular, are assumed to be milling masses of sameness. Perhaps the idea of them as automatons is part of what we find so terrifying about swarms of locusts or bees: each individual is seen as interchangeable with every other, so that killing one has no effect on the rest of the group. They just press on, relentless zombies in our fields and kitchens.

  And yet, as with so many other stereotypes about insects, this one turns out to be wrong. They do have personalities, or versions of them, which leads us to question not only the function of individual differences in animals, but in ourselves. We may take pride in individuality, but what is it for? And if being individuals doesn't set us humans apart, what does?

  Waspishness in Wasps and Boldness in Spiders

  ALTHOUGH psychologists can argue endlessly over definitions of personality, most of those definitions contain some version of individuals showing consistent differences in how they feel and behave. Someone who is aggressive today will be aggressive tomorrow, and aggression in the boardroom means aggression on the basketball court. We also talk about temperament, the predilections that seem to be present when we are born and that shape the formation of personality later on; a fussy infant may become an anxious adult. Sam Gosling, a psychologist at the University of Texas who studies personality in animals, notes, "In some cases, the word temperament appears to be used purely to avoid using the word personality, which some animal researchers associate with anthropomorphism."

  It is true that having a personality seems to imply that one has emotions, a slippery slope when referring to animals, although many early researchers, including Charles Darwin, had no trouble with making the leap. Darwin wrote an entire book on the topic, titled The Expression of Emotion in Man and Animals, and while he concentrated mainly on mammals and whether, for example, baring the teeth in dogs had its counterpart in human sneers, he did not exclude insects: "Many insects stridulate by rubbing together specially modified parts of their hard integuments. This stridulation generally serves as a sexual charm or call; but it is likewise used to express different emotions. Every one who has attended to bees knows that their humming changes when they are angry; and this serves as a warning that there is danger of being stung."

  Far be it from me to contradict the founder of evolutionary biology, but I don't see it this way. Just because a beekeeper—or Darwin—can predict that a bee is going to sting doesn't mean said bee is flooded with rage. It just means that the beekeeper is skilled at reading the bee's signals, like a weather forecaster knowing when a storm is coming because of the quality of the wind and clouds. Animist beliefs and poetic license aside, we don't conclude that the storm is angry either.

  Like most modern biologists, I think insects have personality but think it is presumptuous, not to mention anthropomorphic, to claim that they have humanlike feelings. It is simply too hard to know what is going on inside another being's mind, even when that being is another human, and it seems safe to say that whatever an ant is feeling, it probably isn't the exact same thing humans feel. We are particularly hampered by the lack of facial mobility in many animals, including insects, which makes them even harder to identify with. It's hard to look into the eyes of a butterfly and feel a connection with the being within. Reading expressions is key to our assessment of mood and, hence, personal characteristics, so the absence of frowns and narrowing eyelids in many species (not to mention the eyelids themselves) means that we must use other cues in assessing animal personality.

  But as I do with so many other aspects of insect life, I find the absence of humanlike emotions both challenging and soothing. Challenging because if insects lack feelings, where do their personalities come from? Insects make us ask more and more exacting questions about them, keeping us from sloppy generalizing that assumes they are just like us. And soothing because the insects exist, complete and lovely, in their own world that works just fine without the rules and assumptions that govern human behavior. We think—we know—we would be horrific shadows of ourselves without emotions, and we assume that our personalities stem from the way we feel. But if insects can have personalities without emotions, we have to look harder for the source of those characteristic differences among individuals. Maybe personalities are just collections of traits, like body shape; one is viewed as heavyset or sylphlike because of the shape of one's limbs, the size of the joints, length of the fingers all working together to give an impression of bulk or slenderness. The personality has different components than the body, but it is all still the same thing, and insects show us a reduction down to essentials once again.

  Not all scientists have been willing to accept that insects lack emotions. Donald Griffin, who discovered the details of echolocation in bats and studied animal communication for much of the last half of the twentieth century, spent the later years of his life trying to convince his fellow scientists that nonhumans—whether dolphins, chimps, or honeybees—can possess what he unabashedly called consciousness. He challenged the prevailing view that consciousness, and by extension true emotion, is so subjective that one can never know if others share it. Instead, he defined consciousness pragmatically, as the "versatile adaptability of behavior to changing circumstances and challenges." By that token, insects certainly qualify, and Griffin was fascinated by the complex communication of social insects such as ants and bees. He dismissed concerns that the small brains and differently organized nervous systems of insects precluded consciousness as immaterial, asking, "What underlies this dogma that only a vertebrate central nervous system is capable of organizing thoughts?...The behavior of some insects is far more flexible and versatile than previously recognized. Perhaps this new behavioral evidence will modify our long-standing conviction that all invertebrates are thoughtless automata."

  I like the idea that we have been underestimating insects, but I think we are on very shaky ground extrapolating our own feelings to beings so different from us. Calling insects conscious, or saying that their variable personalities mean they are much like people runs the risk of not paying attention to what they are actually doing, and instead assuming that they are little people in chitin suits. In the long run, I find it more rewarding to see them as insects, and leave the question of their awareness alone.

  Scientists therefore simply rely on the outward behavior of an animal, often under controlled experimental circumstances, to tell them something about its personality. If you place a mouse in the middle of a bare room, is it likely to explore, or huddle in a corner? Does another mouse do the same thing? And if one animal is an exploratory type, does that mean it is also likely to be exceptionally aggressive toward other members of its species? It turns out that it does. The "bold-shy continuum," with some individuals eager to explore and others more risk averse, has been documented in several kinds of animals as well as humans, with evolutionary biologist David Sloan Wilson providing some of the la
ndmark research on the topic. He points out that it is important to remember that being shy, whether in people or sunfish, his favorite study system, is not equivalent to being a loser; in other words, there is something more going on here than just dominance over food or nest sites. Instead, animals take their place on the continuum independent of other determinants of dominance, for example, how large they are and, hence, how likely to win a fight.

  Over the last few years, biologists have also noticed that some individual animals, whether they are fish, ferrets, or fruit flies, tend to show predictable suites of traits, not merely characteristics such as boldness or shyness during a single event. The predictability can happen in two ways. First, an individual that is, say, bold when faced with a predator will also be likely to be aggressive and attack another member of its species, so that its behavior under one set of circumstances predicts a different kind of behavior under another. Second, an animal that is bold today will be bold tomorrow, and one that hangs back will hang back all the time. In another effort to avoid anthropomorphism, or perhaps just because of a fondness for jargon, scientists often refer to these repeatable clusters of traits as behavioral syndromes, a phrase that evokes a bit of the pathological to me—are there behavioral syndrome support groups? Regardless, biologists do use the terms boldness and shyness to refer to animals, particularly fish, for some reason, and bold sunfish are those that are more likely to inspect a predator introduced into their tank, as well as acclimate more quickly to being in the lab and forage more voraciously. These behavioral characteristics can have long-ranging consequences; the bold and shy fish even differ in the parasites they harbor, probably because the different activity levels mean that each type hangs out in a slightly different environment and is exposed to different diseases.