Sex on Six Legs Read online

  What about Wart's ants? Contrary to his experiences, they too can recognize individuals, although unlike the wasps, they lack the distinctive facial or other body patterns used to tell one six-legged companion from another. Instead, ants use chemical signatures, individual odors that ants produce on their external skeletons. We have known for a long time that ants as well as many other insects use such chemicals as general news bulletins—"I am one of you; let me through," or "Female here, sexually available till six"—but had always assumed that such rough categories of signals were the limit of their abilities. But Patrizia D'Ettorre from the University of Copenhagen in Denmark and her colleagues wondered whether ant queens in one species, at least, might do something similar to what the paper wasps do.

  Most ant colonies have a single queen, who settles into a life of fecund bliss after a single mating flight in which she left her home nest, mated, and then spurned any further gallivanting by chewing her own wings off and digging a chamber for her eggs underground. But in a tropical ant species called Pachycondyla villosa, which lives in forests from southern Texas to Argentina, several of the young queens (older literature actually refers to them as princesses, though this terminology is not seen much any more) band together to make a nest in a bit of rotting wood and form a society with a dominance hierarchy and division of labor among the members. As with the wasps, it stands to reason that sorting out whose turn it is to take out the trash would be easier if the ants could tell each other apart. D'Ettorre tested this idea by collecting some of these new queens in Brazil and allowing pairs of them to establish a dominance relationship in the lab. The ants fight by biting, stinging, and boxing with their antennae until one party backs off. Then each queen was allowed to interact with either her former companion or an unfamiliar female. In some trials, D'Ettorre anesthetized the ant her subjects were given to ensure that it was really an individual odor cue, and not just generally aggressive or submissive behavior, that could be used to distinguish one ant from another. In all cases, both the dominant and subordinate queens recognized their former partners. Chemical analysis of the ants' exoskeletons showed no relationship between any particular compound and whether a queen was dominant or subordinate, confirming that the ants were not simply reacting to a generalized "alpha ant" smell. What was even more astonishing was the ants' memory: even after 24 hours of separation, a hefty interval for an animal that lives just a few weeks or months, the queens remembered their previous encounters and behaved accordingly when the two females met (whether there was any frantic internal searching for identity, a kind of ant version of "You smell so familiar but I just can't remember who won when we were together," wasn't discussed).

  Finally, what does being able to distinguish a tiny blob of black or yellow, and remember who has which variant, mean about the brain of the insects that exhibit such a sophisticated ability? In many animals, the part of the brain controlling a much-used behavior is comparatively larger than in species that seem to need it less; thus, for example, bats and owls have disproportionately large portions of their brain devoted to hearing. Neurobiologists Wulfia Gronenberg and Lesley Ash checked out Tibbetts's wasps, as well as other closely related species, and found that being able to recognize faces didn't mean having a larger brain or larger visual centers. Interestingly, the wasps with the recognition abilities had smaller olfactory centers. Another part of the brain with the rather peculiar name of mushroom body was larger than expected, but the difference was quantitative rather than qualitative, suggesting that such a capability is nothing that unusual among wasps, and that similar abilities may be discovered if we simply look for them.

  Personalities and Evolution

  ALTHOUGH individual variation in animal personalities is a somewhat novel idea for biologists, variation itself is not, being the stuff that underlies evolution. Natural selection acts by some variants reproducing better than others, leading to a preponderance of the fitter genes in the population. But this seems like a paradox in the consideration of personality as consistent differences in behavior: if individuals are different, don't some of them perform better than others? And if so, why haven't the more successful ones come to outnumber the less successful ones, so that we are left with only those personality types that are optimal for their environment?

  This question is part of a much larger one, namely, what maintains all the tremendous variability that we see in nature. It's all very well and good to natter on about snowflakes, but living things are far more distinctive. Mutations, changes in DNA that occur spontaneously or as a result of environmental forces such as radiation, supply the raw material for evolution to act upon, of course. But mutations are just the original source of variation; differences among individuals persist in populations over many generations.

  Scientists have a number of theories about how genetic variation is maintained in populations, ranging from the simple notion that selection may not have had a chance to weed out loser genes in some cases, to elaborate ideas about interactions among the genes that happen to be linked together on the same chromosome. Many of these explanations apply to the maintenance of different personalities, too, particularly the idea that advantages and disadvantages trade off against each other. Take the spider femme fatales, for example. Being exceptionally eager to snag a passing fly means that you are more likely to survive another day, which is obviously favored by natural selection: you get moved up a notch on the "likely to live long enough to have babies" scale. But being too rapacious in your treatment of a potential mate might mean lower likelihood of getting enough sperm to fertilize your eggs, which tips the balance in the other direction. On the other hand, a more suave approach to mates may be irretrievably associated with a more lackadaisical feeding style. Each personality type has its pluses and minuses under different circumstances, and they can all coexist because they each make trade-offs in different ways.

  Of course, having a particular set of personality characteristics doesn't necessarily mean giving something up. Some individuals are just all-around winners, and if a behavior is advantageous all the time, then the individual exhibiting it makes out like a bandit and never pays the price. Being particularly active, for example, might mean that an animal finds more food, is more likely to be chosen as a mate, and is first in line for shelter when a storm threatens. Although our Puritanical sides may argue that everything has its price, sometimes that price is negligible. In cases where a trade-off within an individual doesn't exist, one might expect that selection would favor those lucky few, and variation might indeed decrease in the population.

  Alternatively, having a particular personality type may be advantageous if your environment is not very predictable. Andy Sihlikens it to investing in the stock market; if you don't have any information on what is going to happen, it may be better to keep your money where it is than try to play the market, a particularly prescient point in today's economy. For an animal, being predator-wary all the time can be a good strategy when the actual likelihood of being eaten is unknown, a kind of better-nervous-than-sorry attitude. If on the other hand one can be reasonably sure that predators aren't lurking, then one can let oneself go a bit more, as it were, and act one way under some circumstances, and another way under others.

  Yet another way that behavioral variation can be maintained is by having the success of some types depend on how common other types are in a population. If a group of, say, water striders is mainly composed of lethargic, cautious individuals, then being a fast-moving brave strider will be advantageous as long as the reckless types are rare, because the rare ones can dart in and grab food while everyone else is just gathering their thoughts. Once the fast movers reproduce and rise in abundance, however, the slower bugs can in turn do well, perhaps because their type is less likely to be nabbed by a predatory spider. Then the slow individuals do better, and so on; both types can persist over time, even if their relative numbers fluctuate.

  Similarly, several researchers, most notably Judy Stamps at
the University of California at Davis, suggest that personality trade-offs can have repercussions for how fast an animal grows and how many offspring it has. If you live hard and die young, but grow quickly and have your children early, you may end up leaving as many genes in the next generation as someone who grows more slowly, dies at an older age, and paced his or her reproduction more prudently over time. In other words, you could have a personality and life history more like a rabbit or one more like an elephant, and still be a member of the same species—an individual with characteristics at one of the opposite ends of the spectrum. Again, both styles can be maintained via evolution. The question is whether having an aggressive or bold personality is linked with a tendency to die sooner or have more offspring, something that bears investigation.

  Another implication of personalities for evolution is that they make behavior less flexible. In an article summarizing recent work on animal personalities, Alison Bell from the University of Illinois said, "Animals do not always change their behavior as much as they should." While that "should" seems a wee bit judgmental to me (who are we scientists to decree endless flexibility among our animal subjects?), remember Ralph Waldo Emerson's admonition that "a foolish consistency is the hobgoblin of little minds." It is nice to think that insects and we have an equal opportunity to show small-mindedness, but what is the cause of this limitation? Bell speculates that it might just be too hard to change one's personality under different circumstances, even if it would theoretically be advantageous to do so; shifting around the hormones and nervous system reactions might require too much retooling of basic physiology. If the same evolutionary costs and benefits apply to human personalities, we may be better able to understand why some apparently counterproductive ways of coping in humans persist, and ultimately, why we have personalities at all.

  Can We Have "A Feeling for the Organism" if the Organism Lacks Them?

  IN EVELYN Fox Keller's 1983 biography of Nobel Prize winner Barbara McClintock, some of the geneticist's success is attributed to her "feeling for the organism," a way of understanding her scientific subjects that transcended traditional scientific data collection. Keller describes how the scientist had to immerse herself in the minute details of her study subject, understand "how it grows, understand its parts, understand when something is going wrong with it." The book, titled A Feeling for the Organism, became something of a symbol of science needing something more than facts and charts, requiring in addition an emotional investment from the investigator that verges on the mystical.

  This all sounds fine and inspirational, until you discover that the subjects of McClintock's fascination are corn plants. Dotty gardeners cooing to their tomatoes aside, identification with anything other than pets and perhaps a few other animals such as wolves or ravens seems like so much New Age claptrap. But according to Keller, McClintock felt that people had a "tendency to underestimate the flexibility of living organisms." If that underestimation is true for corn, it is doubly so for insects. The idea that they are all alike, with identical reactions and identical lives, used to be unquestioned, as T. H. White illustrated. Now, though, we know better. The famous entomologist Vincent Dethier, author of the masterful book To Know a Fly and discoverer of many important aspects of insect neurobiology, fretted about the likelihood that his subjects had internal lives. In a 1964 essay about the continuum between insect and vertebrate brains, he said, "Perhaps these insects are little machines in a deep sleep, but looking at their rigidly armored bodies, their staring eyes, and their mute performances, one cannot help at times wondering if there is anyone inside." Nearly half a century later, and with the appropriate caveats about personality sans expression, the answer seems to be yes.

  Chapter 4

  Seinfeld and the Queen

  IN Bee Movie, Jerry Seinfeld plays a slacker honeybee, yearning for a life beyond the tedium of the factory. His portrayal of a social insect as male is as glaring in its inaccuracy as in its ubiquity. No one, including me, expects movies to be faithfully accurate in all their details. But there are errors and errors, poetic license versus jarring ineptitude, bloopers versus downright stupidity. Talking animals is one thing, but getting it wrong about honeybees is on a par with portraying astronauts in a universe where the earth revolves around the sun, or TV doctors who are worried about anemia due to a lack of lead in the blood instead of iron.

  And it goes beyond an expert's superiority at having "gotcha," more than the fun of discovering a telephone in a pre-Bell movie. The way I see it, there are at least two problems with exhibiting such flagrant ignorance about the sex of the social insects. The first is that it perpetuates a skewed vision of the world and its sex roles, a vision that can end up doing our own society some harm. The second is that if you assume everything in the insect world is the way it is in our own species, you miss out on stuff. And in sex roles, as with many things about insects, the truth is much, much more interesting than fiction.

  His Thighs with Sweetness Laden

  NOT KNOWING that virtually all the ants or honeybees that one sees are female is nothing new. The phrase in the subtitle above comes from a poem by Charles Stuart Calverley, a mid-nineteenth-century Englishman said to be the father of the "university school of humor," a designation that as a professor I find compelling yet enigmatic. He wrote several books of poems, including Fly Leaves, which contains the following lines:

  When, his thighs with sweetness laden,

  From the meadow comes the bee,

  Even Benjamin Franklin fell into the stereotype; a letter he wrote to a woman he was apparently courting contained the following lines from a poem by William Pulteney:

  Belinda, se, from yonder Flowers,

  The Bee flies loaded to his cell:

  Can you perceive what he devours?

  Are they impair'd in shew or smell?

  Franklin and Calverley, as well as the people from Disney, Pixar, and various other movie studios, were following in a tradition present since at least the ancient Arabs and Greeks, who believed that a king bee, or "bee father," in the case of the former, was in charge of the hive and that the followers were probably male as well, though this latter point was the source of some debate. The Greeks were able to distinguish a category of bees, the drones, that were larger than the workers, but although they disapproved of the bees' apparent laziness (the drones hang around the hive until their mating flight and are fed by the workers but do not collect nectar or pollen), they could not determine the drones' sex. Part of the confusion seems to have been that the Greeks were well aware of the stinging ability of bees and found it impossible to believe that any animal bearing such a weapon could be female.

  Similarly, on viewing the fierce defense of the hive exhibited by most social insects, including honeybees, many Arab cultures likened the colony to an army, which naturally implied a military rule, with males as both officers and soldiers. (The stinger is a modified ovipositor, or egg-laying structure, but the workers are generally unable to reproduce.) Aristotle tried to reason out the problem but ran into difficulty because if the stinging bees, the workers, were male, that would have suggested that the drones were female, and he was unable to accept the idea that the males in a society did all the work of taking care of the young. He eventually concluded that bees might have the organs of both sexes in a single individual, as do many plants, but then was further flummoxed by the lack of reproduction on the part of any individuals but the queen (or leader, as he called it).

  In Henry V, Shakespeare refers to "The lazy yawning drone," as well as the king of the bees, again without any hint of recognition that the shiftless members of the hive were male. Writing in the nineteenth century, Calverley, it turns out, actually should have known better, because the sex of the queen was ultimately determined in the late 1600s. Several writers and beekeepers had guessed at the truth, but Jan Swammerdam, a Dutch microscopist, is generally credited with demonstrating that the individual assumed to be the king had unmistakable ovaries and was respons
ible for generating the other bees in the colony. Swammerdam published two books with breathtakingly detailed drawings of the anatomy and life cycles of bees and ants, among other things, some of which were not equaled until the twentieth century. He had to manufacture his own miniature tools and adapt the primitive magnifiers of the day for his own use. He is said to have publicly dissected a purported king bee in 1668, an event I must confess I have a hard time imagining. Admittedly, learned men had a different means of spreading knowledge back then, but it is entertaining to picture the way in which news of the impending feat might have spread: "Hey, did you hear? Ol' Jan Swammerdam is cutting open a bee next Tuesday! Who knows what peculiar structures he will reveal! Let's go watch—I'll buy the mead." Do you suppose he sold tickets?

  In any event, Swammerdam correctly distinguished the anatomical differences among the larvae, or young bees, and the drone, worker, and queen. The next puzzle was to determine how exactly the queen produced the other types, since no one had ever seen bees engaging in sex. Here he was not so prescient. He suggested that the sperm from the drones somehow wafted through the air and the odor then was powerful enough to impregnate the queen, a theory called aura seminalis. Swammerdam noted the distinctive smell of the drones in the colony and assumed that this stench was powerful enough to inseminate at a distance. Why he was content to speculate rather than test his theory is not clear, given his modern, experimental approach to the rest of his work. At one point he even suggested a possible test of the aura seminalis idea, in which one would determine "whether the female Bee, enclosed in a little net made of fine thread, or in a small glass vessel covered with a piece of fine linen, or in a box with holes in it, could be impregnated by the bare scent of the male."