Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World - Marlene Zuk (2011)

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 responsible 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."

In Swammerdam's defense, the mating process in honeybees was not clarified for a few hundred more years, although some eighteenth-century scientists had noticed that a queen bee sometimes returns to her hive with the genitalia of the drone still attached to her reproductive organs. Finally, in the mid-1900s, naturalists discovered drone swarms, groups of virgin male bees that congregate in small areas near hives. At the right time of year, if you know where to look, you can find the would-be suitors by listening for their humming. My college entomology professor took us to one such gathering, and although we could hear but not see the bees, when he flung a pebble into the air above our heads it was instantly pounced upon by the drones. The young queen flies into the swarm and is pursued by the males; as the queen flies faster and farther, she leaves behind all but the most ardent males. Finally she mates with one or more of the drones, who die immediately and fall to the ground while she carries their sperm back to the hive.

Sex and Honey

PARALLELS between bee and human society and gender roles—or lack thereof—have been popular for a long time. The bees' communal life, industry, and apparent self-sacrifice for the good of the colony were held up by many ancient civilizations as models to which humans would do well to aspire, and beehives have served as symbols for groups as disparate as Masons and Mormons. Once it was established that the worker bees did not mate, their chastity was also suggested as an inspiration to women. After the queen bee's sex was discovered, writers such as Charles Butler, author of The Feminine Monarchie, published in the early seventeenth century, began to shape their newfound knowledge into a form more acceptable for the social mores of the time. Butler approvingly noted that the drones had a louder voice than the female workers, just as the rooster's crow is louder than the sounds made by hens, but seems to have conveniently ignored the "piping" noise, much more pronounced than the humming of the drones, produced by queens shortly after they emerge as adults from their waxen cells. Piping queens also show another less than feminine trait when they attempt to kill any other queens emerging in the colony at the same time, but this behavior also seems to have gone unremarked. Similarly, queen bees were described by Richard Remnant in his 1637 writings as "gentle and loving," though it is hard to see a female that dispatches rivals by biting their heads off and renders her subjects sterile as being particularly benign.

It is possible that some of the sex role confusion about bees was deliberate; scholars have questioned whether, for example, Benjamin Franklin was unaware of the current state of knowledge about the sex of the worker bee, or whether he might have changed the pronouns from the original song to suit his purposes. I am more inclined to attribute the errors to ignorance. My own admittedly unofficial polls show that, far from being common knowledge, many of my students and those I meet at other universities have no idea that worker bees and ants are female. After my lecture on army ants, the legendary voracious consumers of everything in their path, a typical exchange with a student will go as follows:

"So, Dr. Zuk, you know about the ants?"

"What about them?"

"Like, you said all the workers were female, but what about the army ants?"

"Their workers are female, too."

"Yeah, but what about the soldiers, the ones you said have those huge jaws and everything?"

"They are female, too."

"So really, the soldiers, they are female?"

"Really." At that point the student usually slouches off, eyeing me skeptically. I always feel that I have let them down, but it's not clear how.

Lest you think this is an American fixation, I should tell you about Yamba the Honey Ant. Honey ants, sometimes called honeypot ants, are found in the arid regions of Australia and a few other parts of the world, where they live underground in a network of chambers and tunnels. While most of the ants are able to leave the colony to look for food, some of the workers have immensely swollen abdomens that serve as living storage vessels for the rest of the colony. They never leave their underground den, and other ants tap on the honeypot individuals to get a drop of food. Native peoples, including aboriginal Australians, dig up the nests to harvest the stored honey.

In central Australia, a children's television show features Yamba the Honey Ant, a cheery character portrayed (with a bit of poetic license) in the red, yellow and black colors of the aboriginal flag. On a visit to Alice Springs, I was encouraged to see that Yamba was accurately depicted with six legs, and I wondered if this faithfulness to reality went so far as Yamba's sex. Alas, it does not; Yamba is firmly a male ant, leaving generations of Australian schoolchildren to grow up with the same misconceptions as my own undergraduates.

Insects, Chromosomes, and Surf City

THE FOCUS on males in films about bees and ants, and our own unthinking assumptions about the sex of animals in nature, may say things about the sex bias in human society. But an even more egregious failing in the error is that it means people don't learn about one of the most amazing things in nature: the sex ratio, or the relative proportion of males and females in a population, and how it evolved. Insects have been essential in our understanding of this fundamental issue in biology, and they also exhibit some of the weirdest maneuvers on the basic theme.

We take for granted that under natural circumstances, roughly equal numbers of boys and girls are born into the world. Indeed, for many species of animals, including people, that is the case, with a sex ratio of 50:50. But why should that be so? If you think about it, from an evolutionary standpoint it seems puzzling that so many males are produced, since of course a single male can impregnate a great many females. In species in which males don't have anything to do with the offspring after mating, which includes most animals and certainly the vast majority of insects, it would seem to be much more efficient to produce a few males to provide the sperm and leave it at that, putting all the rest of one's reproduction into daughters, the real producers of the next generation. Why, then, are equal sex ratios so ubiquitous?

If you remember high school biology and a bit about sex chromosomes, you might think the answer is a consequence of how sex is determined when sperm meets egg. Humans and other mammals all possess two sex chromosomes: in females, two copies of an X, and in males, a single copy of the X and a smaller Y chromosome. Since only one of the sex chromosomes goes into each sperm or egg cell, half the sperm make daughters, with two Xs, and half make sons, with one X and one Y. Ipso facto, you get an equal distribution of males and females. Although birds, butterflies, and a few other animals have the situation reversed, with males produced from two Z chromosomes and females from a Z and a W, the same process takes place. The analogy with tossing a coin has been made so often that you have to wonder whether, if we commonly had more than two sexes, we would all be using three-sided coins.

But satisfying though this explanation may seem at first glance, it is ultimately not the answer to the question of equal sex ratios, as Mike Majerus points out in his book Sex Wars. First, it's quite possible that the mechanism for determining which chromosome goes with which sex evolved as a means to get to the optimal sex ratio, not beforehand; as with the coins, it would be fallacious to argue that we have the two options of heads and tails on our coins so that we can calculate the sex ratio. Second, as I will describe in more detail below, many animals have the same sex determination mechanisms we humans have but still produce wildly biased sex ratios. And finally, even though "our" XX/XY (or ZZ/ZW) system is widespread, numerous other ways to determine maleness or femaleness are found throughout the animal kingdom, including special genes and the temperature at which eggs are incubated (in many kinds of turtles, for example, cooler nest temperatures yield male babies and warmer ones, female babies). So the equal sex ratios in turtles, at least, must arise from some other source.

As with so many other ideas in biology, Charles Darwin both identified the problem and proposed a plausible solution. Many biologists overlook his original suggestion because it appeared in an early edition of The Origin of Species and was retracted in the later ones. Sir R. A. Fisher, a British geneticist and statistician, is generally credited for the breakthrough. Either way, the key is to think about things, not from the standpoint of what is most efficient for the population or species as a whole, but from a gene's eye view. What will make it more likely that a gene will be perpetuated in future generations, the key to evolution?

Say that, indeed, fewer males than females are produced in a hypothetical population of animals, as it was in Jan and Dean's 1963 song "Surf City" ("Two girls for every boy"). Each male fertilizes multiple females, so more copies of each male's genes appear in subsequent generations. That means that having sons is advantageous, so any tendency to do so will be favored by natural selection. Eventually, though, more males than females appear in the population, and then those males are not in nearly as happy a circumstance. Because each child can only have one mother and one father, some of the surplus males must go without mates, and then parents who produce daughters, rather than sons, are at an advantage. That bias then leads to an abundance of females, with the same benefit to being a male that we started with. This kind of seesaw evolutionary process across the generations is called frequency-dependent selection, and it is easy to see that it makes a 50:50 sex ratio the equilibrium that a population settles at, all else being equal. "Surf City," idyllic though it may have sounded to the beach crowds of the 1960s, just isn't a viable way to run a species.

My Sister, Myself

SO HOW do the honeybees get away with having female-dominated societies? The drones comprise less than 5 percent of the total number of bees in the hive, so they clearly violate the equilibrium ratio. In many other insects, although the sex ratio is not always so extreme, a preponderance of females is the rule. The reason the bees can do what we can't has two sources: the way sex is determined, and a special violation of the "all else being equal" clause above.

Unlike the species discussed above, bees, wasps, and ants don't make males and females using combinations of special sex chromosomes. Instead, males are produced from unfertilized eggs, and hence have only one copy of each chromosome, while females have a more normal (to us, anyway) complement of two copies, because the queen produces them by fertilizing eggs with the sperm of the hapless drone or drones she left behind when she entered the hive to start her monarchy. Again unlike humans, queens of social insect colonies can store sperm for years, doling out a son here, a batch of daughters there. The daughters may become workers, in which case they are sterile, with undeveloped ovaries, or future queens, in which case they are cosseted by their sisters and fed exclusively on royal jelly, a nourishing compound (for bees, anyway) that alters hormone levels and facilitates ovary development. (Little or no evidence exists that royal jelly, whether applied topically or eaten, does anything for humans besides diminish their pocketbooks.)

This genetic peculiarity means that in cases where a queen mates with a single drone, her daughters are more related to each other—their sisters—than they are to hypothetical daughters of their own. To understand this, recall that in humans and other species with XX/XY sex determination, offspring get half their genes from their mother and half from their father, making siblings half like each other as well. Because each sperm and egg cell contain only half of each parent's genetic complement, in species such as our own, each sibling has a 50 percent chance of getting any one chromosome from the parent. But because male bees have only one copy to begin with, all the sisters get the same genes from their father. They get the usual 50 percent from their mother, giving them a total of 75 percent of their genes in common. The queen, on the other hand, shares the usual 50 percent of her genes with either her sons or her daughters.

This unusual sisterly closeness is thought to play a role in the extreme altruism exhibited by many of the social insects, but it also is important in the sex ratio. I have been acting as if sex ratio is concerned only with numbers, but in fact, the mere number of males versus females is only part of the story. What really counts is the investment in terms of energy that is made in either sex. Say that females "cost" less to produce—perhaps they are smaller than males, and so fewer calories go into manufacturing them than are required to make the same number of males. Natural selection will favor making more girls than boys, because each girl is cheaper, but the overall investment in each sex is still equal.

For the bees and ants, the asymmetry in how closely related sisters are compared with mothers and offspring means that the evolutionary payoffs for producing different sex ratios are different for the workers than they are for the queen. The workers' only chance at perpetuating their genes is via the future queens and drones, or males, produced by the queen, because workers are sterile. The queen's genetic future lies in the same individuals, but the two differ in what will most benefit each. From the workers' perspective, more of their genes will be passed on if more energy is allocated to the future queens, their sisters, than to their brothers, because they share only 25 percent of their genes with the latter, a third as much as they have in common with their sisters. The queen, in contrast, is equally related to her sons as her daughters, so an equal ratio of investment in the sexes would benefit her the most.

Bob Trivers, an evolutionary biologist at Rutgers University, was interested in determining who "won" this potential conflict between the workers and the queen in the sex ratio of the social insects. With the assistance of Hope Hare, he painstakingly weighed the future reproductive individuals in the nests of a number of ant species. If the queen was in charge, as it were, and her reproductive interests are paramount, one expects that the weights—a reasonable gauge of investment—of the male and female future queens and males would be equal. If the workers prevailed, however, one expects a bigger investment in the young queens, by a factor of three, since the sisters are three times more closely related to each other than to their brothers. It turned out that the combined weight of the males in the nests was just about exactly one third of that of the future queens, supporting the idea that workers control the sex ratio of the colony. That discovery in turn means that insect societies, the most complex social systems on earth, are not dictatorships, but are controlled by a Machiavellian network of alliances and favors exchanged.

Incest and the Solution to Physics Envy

THIS successful application of theory to nature was only one of many triumphs of sex ratio theory as it applies to insects; arguably, the ability to predict with quantitative precision the relative numbers of males and females in an insect group is one of the most impressive confirmations of the operation of natural selection. Ecologists and evolutionary biologists often have to settle for qualitative predictions about the real world: we can say with assurance that a population will grow if more food is available, but exactly how much? Under most natural circumstances, too many other variables are at play to make precise predictions from such a biological hypothesis; the population's growth rate depends not only on food but also on, for example, the likelihood that disease will infect its members, or the abundance of predators in the neighborhood. This uncertainty has led to what people sometimes call "physics envy," the longing for the kind of mathematical confidence seen at least much of the time in the so-called hard sciences.

But physics envy can be cured by a dose of tiny parasitic wasps and an understanding of sex ratio theory. The wasps in question lay their eggs on other living insects, usually caterpillars or fly larvae, and the young wasps then develop inside this live food source until they are ready to become adults themselves. Just after the wasps become sexually mature, they mate, still on their host, and then the fertilized females go off to find victims of their own. Each caterpillar can support only a few females' offspring at most, which means that the young wasps find themselves in a very restricted universe in terms of dating opportunities. It's like going to a singles gathering with just your brothers and sisters and maybe the kids from the house across the street, and knowing you will have to find your lifetime mate from among only those individuals. Although inbreeding, or mating among relatives, has genetic penalties in many organisms, including humans, in the wasps it does not carry the same consequences, and they will mate quite unconcernedly with their siblings.

The mother wasp laying her eggs on the host has the same evolutionary problem as other organisms: how best to leave the most genes in the next generation. If she is the only individual parasitizing a particular caterpillar or maggot, she will get the most bang for her genetic buck by producing only enough males to fertilize their sisters, and making most of her offspring female. Making more males will only produce competition among them for the same mates, which won't do the mother wasp any good. The more additional females that use the same caterpillar, however, the more advantageous producing more sons becomes, because those sons can then compete to fertilize the daughters of those additional females. So one would expect the sex ratio to become increasingly male biased as the competition heats up.

Starting with work published by the evolutionary biologist W. D. Hamilton in 1967, scientists have worked out exactly what sex ratio a female parasitic wasp is expected to produce under a variety of circumstances, such as the number of other females laying eggs in the same host. And nature has been astoundingly obliging in supporting the predictions, down to the last egg. Much of the original research was done in the lab, where the wasps can be induced to lay eggs on fly larvae in dishes, but recent DNA analysis of over three thousand offspring from forty-seven mother wasps collected in the field in Europe confirmed that the equations can be used to predict life in the real world. The theory even applies to the one-celled organisms that cause malaria, which also come in two sexes. Take that, string theory.

A Good Year for Sons

ALTHOUGH on average the number of men and women is roughly equal, the availability of either sex depends on the situation. You will be more likely to find a single man in a bar in Alaska, more apt to meet women at a convention for nurses. As it happens, these concerns about the sex ratio among humans also affected the development of another major theory about sex ratio in nature itself.

It all started when Bob Trivers, the biologist who worked out the ratios of reproductive individuals expected within ant colonies that I discussed above, was a graduate student at Harvard. Trivers was a teaching assistant for a popular course in primate behavior, and as he relates in his collected papers, he had a mathematics student named Dan Willard who took the course as a way to meet women. The math graduate program at Harvard, as elsewhere, was rather like the aforementioned Alaskan bar in terms of its sex ratio (I assume, without really knowing, that the resemblance stops there), but the primate behavior class of nearly three hundred students was about two-thirds female. Trivers never divulges whether Willard's social hopes were fulfilled, but after a lecture about why the sex ratio is usually 50:50, Willard came up with an idea that the two of them later published as a highly influential paper in Science.

Like many keen insights, this one seems simple once you hear it. Having offspring is costly, in the sense that it requires energy from the mother to produce eggs or babies. And as pregnant women the world over are acutely aware, the condition of the mother affects the condition of the baby, often for a long time after birth. Even among insects, better-nourished mothers can often produce larger eggs that in turn develop into more robust larvae. Although of course it would be ideal to always be in the best shape possible and produce the highest quality offspring a mother can, the situation doesn't always allow mothers to be in that tiptop condition.

Trivers and Willard reasoned that the consequences of producing a baby that is of less than optimal condition will differ depending on the sex of that baby. Because males in many animal species compete vigorously for mates, only males of the highest quality are expected to be successful in fertilizing a female. Producing a weakling son is therefore unlikely to yield any reproductive payoff for the mother. On the other hand, if one's son is very successful in combat with other males, he can potentially sire many more offspring than a single female, even one in the best condition. Even a daughter in poor condition, however, will almost certainly find a mate and reproduce. So Trivers and Willard predicted that when circumstances keep the mother from pouring a lot of resources into her offspring, she would be more likely to have daughters than sons, and vice versa for mothers lucky enough to be at the top of their game.

The mechanism behind such a sex bias is not entirely clear. No one, least of all Trivers and Willard, suggests that animals alter the usual method of chromosomal sex determination. But many more eggs are fertilized than end up implanting in the uterus or developing into offspring, and it is possible that embryos may be selectively retained or discarded depending on the mother's condition. This does not require a conscious decision on the part of the mother, of course, but selection may have favored implantation of a male or female egg only if, say, her hormone levels reflect a particular level of nutrition.

The Trivers-Willard effect has been demonstrated in a wide range of animals, from deer to fish to birds, and may even operate in humans. A 2008 study of 740 British mothers found that the women were more likely to give birth to a boy if their diets were more nutritious around the time they had conceived. The bias was not huge—56 percent sons among the mothers that ate the most, versus 46 percent sons among the least-nourished women—but it suggests that more than chance may play a role in the sex ratio even in our Western societies. These insights in humans wouldn't have come about if we hadn't had insects, with their wildly variable lives, as test cases.

Insects do not become pregnant, of course, although some retain the eggs inside or on the mother's body after they are produced. Furthermore, among many insects, large females are favored by natural selection because they can lay more eggs. Good conditions might be expected to cue the production of daughters, rather than sons, to take advantage of the resources necessary to manufacture a robust future mother. Indeed, among many parasitic wasps and flies, the sex ratio is biased toward daughters when the host maggot or caterpillar is large, and toward sons when the host is puny and provides less nourishment for the growing parasites.

Finally, the sex ratio in some insect species can fluctuate wildly, even over the course of a very short time. A Polynesian butterfly had only 1 percent males in 2001, due to an infection by bacteria that selectively kill male embryos. But just 5 years later, researchers found a nearly 50:50 sex ratio on some of the islands where the butterfly occurs, even though the bacteria were still present. Selection apparently acted to reduce the male-killing ability of the bacteria, probably because producing males was enormously advantageous in the highly female-biased populations.

See what you miss if you assume that Jerry Seinfeld makes a good bee?