So Two Fruit Flies Go into a Bar - Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World - Marlene Zuk

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

Chapter 6. So Two Fruit Flies Go into a Bar...

AS SOMEONE who works on sexual behavior in animals, I've grown used to getting a lot of off-the-wall questions from curious members of the general public. Topping the list is homosexuality and whether it occurs in species other than our own. (Another inexplicably popular area of inquiry is whether animals exhibit oral sex. I still have no idea why people want to know the answer to this, and have always been afraid to ask.) And any media mention of homosexual behavior in animals always garners lurid headlines and stimulates acrimonious on-line debates. In 2007, for instance, news that scientists induced homosexual courtship in male fruit flies by changing the levels of a chemical that is key to many processes in the nervous system was greeted with predictable tabloid hyperbole: "Scientists make fruit flies gay, then straight again." On science and gay rights blogs alike, discussion raged about whether this meant that a drug altering sexual orientation would, or should, be developed by the demon Big Pharma. Others trotted out well-worn arguments about whether sexual orientation is learned or genetic and about its existence elsewhere in the animal kingdom, and then meandered into why places with large contingents of gays—such as San Francisco and Boulder, Colorado—are often such nice places to live.

Similarly, every time the issue of gay marriage rears its head, animal homosexuality comes up, in part because arguments against gay marriage often invoke phrases such as "natural order," "natural law," or "crime against nature," which make it, well, natural to wonder about whether birds—and even the bees—do that, too. And marriage aside, animals have always featured more generally in discussions of how "natural" homosexuality in humans might be, although which side their behavior is used to support differs. On the one hand, some gay activists have pointed to the widespread occurrence of same-sex courtship among animals from penguins to whales as evidence of it being part of the natural spectrum of acceptable behaviors. Animals are also sometimes used to bolster the argument that sexual orientation is not a choice but a genetically influenced, or even genetically determined, trait. Some conservatives, on the other hand, feel that animals exhibiting a distasteful behavior just underlines its debased nature. Simon LeVay, a prominent researcher in the genetics of sexual orientation, throws up his hands: "The question of whether animals engage in same-sex sexual behavior has been debated for centuries, most often in the context of efforts to stigmatize homosexuality. Three classes of answers have generally been offered: 'Animals don't do it, therefore it's unnatural'; 'Animals do do it, therefore it's bestial'; and 'Some animals do it, and those are the unclean animals.'"

At some point in the argument someone inevitably says, as if no one else would have ever thought of it, that animals do all kinds of things we don't want to emulate, for example, eating their young or abandoning their elders. The implication, presumably, is that what animals do is sometimes repugnant, so we should ignore their behavior when considering our own. While it's certainly true that we don't need to use other species as role models for behavior to emulate, animals need not mirror all aspects of our lives to be useful in teaching us about some of them. We use animals as experimental models for many parts of our biology that they do not possess in their entirety. We can learn a great deal about how babies grow into adults by observing rats, even though rats never learn to drive or go to college. And we are fascinated with the things that animals do that seem so uncannily similar to what we do, as anyone who has watched a mother monkey expertly sling her baby on her hip before setting off for a nearby shrub can testify.

Insects play a special role in our use of animals to help us understand ourselves, as I argue throughout this book. Because they are rarely cared for by their parents, and usually live relatively solitary lives without the input of others, the behavior they exhibit as adults is largely controlled by their genes. And although we are increasingly discovering how flexible their behavior can be, as I discuss in the chapters on insect learning and personality, it's still a safe bet that if a bug seems to be homosexual, it didn't get that way because of an absent father or overbearing mother messing things up during its larval stage. Their behavior is thus stripped down to its essentials, a handy tool for looking at complex actions.

So what do we know about homosexuality in animals, particularly insects? And what does that tell us about sexual orientation in humans? The results of studies showing same-sex behavior in flies, beetles, and butterflies are coming in every day. This news is significant for several reasons, but it is meaningless for another one, and that one is the reason that many people are interested in it in the first place.

Lowering of Moral Standards in Butterflies

AS BRUCE Bagemihl points out in his 1999 book Biological Exuberance, researchers have been noticing same-sex behavior in both wild and captive animals for many years. This is not to say they were always happy about it or viewed their discoveries dispassionately; a scientist greeted the sight of male bighorn sheep mounting each other and forming long-term homosexual bonds with: "I still cringe at the memory of seeing old D-ram mount S-ram repeatedly.... To state that the males had evolved a homosexual society was emotionally beyond me. To conceive of these magnificent beasts as 'queers'—Oh, God!"

Even lowly invertebrates are subjected to such dramatic responses; the 1987 volume of the Entomologist's Record and Journal of Variation contains "A Note on the Apparent Lowering of Moral Standards in the Lepidoptera [butterflies and moths]," a gem I have read several times, still without being sure whether it is meant to be tongue in cheek. In it, the author laments, "It is a sad sign of our times that the National newspapers are all too often packed with the lurid details of declining moral standards and of horrific sexual offences committed by our fellow Homo sapiens; perhaps it is also a sign of the times that the entomological literature appears of late to be heading in a similar direction." He then goes on to detail observations of male Mazarine blue butterflies, a lovely European species, vigorously and persistently courting other males, particularly when the object of their attentions had just emerged from the chrysalis, despite the ready availability of females. The note concludes with the reassurance that several heterosexual pairs—referred to as "normal"—were also seen, thus indicating that "at least some individuals had the furtherance of the colony at heart and the appearance of the colony next year is thereby assured."

Admittedly, The Entomologist's Record is not the most prestigious or widely cited of journals and contains quite a few other anthropomorphic articles, such as the poignantly titled, "Do Copper Underwings (Amphipyraspp.) Crawl Away in Order to Die in Peace?" Nevertheless, same-sex behavior in animals, whether sheep or butterflies, seems to bring out this kind of histrionic reaction in those who observe it. And Bagemihl points out that we are probably seeing only the tip of the homosexual iceberg, since many more researchers may be seeing similar behavior in their study organisms but ignoring it or dismissing it as a meaningless aberration.

Because insects do not invite the same identification or anthropomorphism as mammals and birds, though, we can at least hope to use them as testing grounds for our ideas without automatically falling back on our biases. Most modern scientists would dismiss the idea that moral standards exist at all in butterflies, much less that same-sex behavior is a sign of them. What kinds of homosexual behavior do we see in insects and other invertebrates?

For example, the males and females of a small spider that biologist Rosemary Gillespie studied in Hawaii do not exhibit any elaborate courtship behavior before mating. Instead, they simply leap at each other, fangs outstretched. If such abrupt amorousness is acceptable to both parties, the fangs become locked together (giving new meaning to the phrase "hooking up"), and the female curls her abdomen around so that the male can insert his sperm-bearing organ into her reproductive opening. A captive pair of males that Gillespie had collected a few weeks earlier exhibited much the same behavior in their container, remaining coupled for 17 minutes. Similar same-sex pairings, usually between males, have been seen in captive and wild beetles, locusts, wasps, and a kind of fly that lives near streams and lays eggs in water lilies.

In the blue-tailed damselfly, females come in three colors, one of which resembles that of males. Hans Van Gossum and his colleagues at the University of Antwerp in Belgium kept male damselflies either with other males or in mixed-sex groups and then allowed the males to choose between a female or another male in a small cage. Males that had experienced the damselfly equivalent of a British boarding school were more likely to then seek out another male and form a pair with him, while the males from the coed environment were more likely to pair up with a female.

To interpret this puzzling result, we need to know some details about the sex lives of this insect group. Mating in damselflies and dragonflies is both distinctive and complex, and because the insects are aerial, one can often see mated pairs flying over the surface of a stream. A male damselfly or dragonfly, unlike other insects (and most other animals, for that matter), actually has two sets of genitalia, one at the tip of his abdomen and the other closer to the center of his body, at the underside of the second abdomen segment. Before mating, the male transfers his sperm from the tip to the more central location. Then, once a male sees a female he intends to mate with, he flies up and grasps her behind the head with his rear appendages in what is called a tandem position. The pair may fly together like this for several minutes or even longer. Eventually, if the female does not reject the male, they land on a plant or some other object and form a wheel: the female bends her abdomen tip to reach the male's secondary genitalia so that he can transport his sperm into her reproductive tract. (I've always thought the wheel looks a lot like a heart, and often show images of paired damselflies to my class on Valentine's Day.) The couple will remain in the wheel position for up to 15 minutes, and the male often accompanies the female after mating is over, still in the tandem position, while the female returns to the water to lay her eggs.

This rather convoluted process means that males can potentially waste a considerable amount of the females' time by persistently grabbing them in midair and chasing them around a pond or stream. Given that the females live only a few days or weeks in most species, and that it's important to find the best place and time to lay eggs, such harassment is more than merely annoying—it can compromise the female's ability to reproduce. The malelike morph of the females in the blue-tailed damselfly and several other species is thought to have evolved to allow the masquerading females to avoid some of the pestering, because males initially at least mistake them for other males and are less likely to bother them. This in turn means that selection will act on the males to make their acceptance rules for whom to court and who to shun a bit more flexible, so as not to miss out on any mating opportunities.

Van Gossum suspects that having this relatively open-minded response to all members of the same species, regardless of sex, means that a certain proportion of male-male pairs is inevitable, even though they obviously cannot increase the reproductive success of the males involved. The idea is that it's better to have a coarse decision threshold and risk accepting some mistakes than to be more discerning and risk missing some actual females. It's a bit like testing for certain cancers, where doctors would rather put some people through unnecessary biopsies and anxiety for a false positive than risk missing some actual signs of disease. In evolution, as in medicine, where to set the bar is not always clear.

Boys Will Be Girls Will Be Boys, Naturally

PEOPLE sometimes conclude from this kind of work that the damselflies, or Gillespie's spiders, or any of the other insects and their kin observed in homosexual pairings are making a mistake, and therefore human homosexuals are likewise in error, some kind of evolutionary fluke. Interestingly, a National Geographic story on Van Gossum's study suggested, "Such flexibility may also lead to genuinely homosexual damselflies." This implies, I suppose, that the damselflies in the Belgian experiments were somehow not really gay, although it's hard to know what the litmus test might be.

Instead, I think it makes more sense to see the flexibility in mating behavior, same-sex courtship and all, as part of the animals' natural repertoire. We cluck disapprovingly over the males' supposed errors, but that represents our misunderstanding of how evolution works. François Jacob famously said that nature is a tinkerer and not an engineer. What he meant was that natural selection doesn't produce perfection; it produces traits that are good enough. We often think of this in connection with our bodies, so that we have spines that are not really adapted to walking upright or immune systems that sometimes overreact to give us allergies to harmless substances, but the slop is part of every system, including behavior.

The chrysanthemum longicorn beetle (Phytoecia rufiventris) is a lovely insect with a ruby red spot on its back and a rust-colored abdomen. It is a pest of chrysanthemums, as the name suggests, and a single female can kill as many as seventy plants by laying her eggs in the stems, which makes understanding the beetles' biology of interest to horticulturalists. Unlike many insects, the chrysanthemum beetle lacks sex pheromones, those come-hither odors often employed as long-distance mate attractants and sex identifiers. The sexes find each other in the first place because both males and females are attracted to plants of a certain height. Qiao Wang at Massey University in New Zealand and his coworkers discovered that the male beetles reacted similarly to males and females when they first encountered them on a plant stem by attempting to copulate. After the male mounts, he engages in a rather complicated and lengthy probing with his abdomen until he can touch a tiny segment of abdomen of the beetle underneath him, and it is only at that point that he can determine whether he has mounted a male or a female. Eventually he disengages from an individual found to be another male, but Wang and his colleagues suggest that "males may 'waste' a lot of time during their reproductive life."

But time wasted is in the eye, or maybe the pheromone glands, of the beholder. Sure, if the beetles had a more foolproof way to determine who was who, they would have more time to feed, or hide from predators, or do crossword puzzles for that matter (what's a nine-letter word for "life-destroying chemical"?). Similarly, if human beings had pelvic girdles that could more easily accommodate a full-term fetus, childbirth would be a breeze and the militant advocates of natural versus medically assisted labor would have to find something else to clash about. But in both cases, evolution didn't produce the best solution, it produced what worked.

Seemingly maladaptive traits may persist because no genes for a more efficient matchmaking technique or a less painful birth process exist for natural selection to act upon. If a male beetle with a genetic mutation allowing him to sniff out females were to crop up, he might be wildly successful, and in time his progeny would outnumber the old models. Maybe someday that will happen, thanks to the vagaries of genetics. In the meantime, as long as we have chrysanthemums for them to plunder, the beetles muddle along. Alternatively, the trait might represent a compromise between competing selection pressures: you can have a good pheromone system, but then your predators can find you, or you can't perform some other essential task. A more capacious pelvis might come at the expense of walking. If the fetus were smaller when it was born, a solution many of our primate relatives opt for, we'd have babies with less brain power. Ironically enough, entomologists often exploit the pheromones of insects by constructing traps that emit an artificial version of that enticing odor that ordinarily means that romance beckons; when the hopeful suitors arrive, they are summarily dispatched. The lack of sex pheromones in the chrysanthemum beetles makes them that much more difficult to lure to their deaths.

A similar delay in figuring out who is male and who is female occurs in a species with one of the most grisly mating habits in the world, the African bat bug. These insects are related to bedbugs, although as the name implies, they ordinarily suck blood from bats in their caves rather than human beings in their beds. Both insects reproduce not via males depositing sperm in the female's reproductive tract but through a process called, accurately enough, traumatic insemination. The male literally pierces the body wall of the female and leaves his sperm to swim through her body cavity to fertilize her eggs. Males always stab the female's body in the same place, and when they do so their organ must pass through a specialized structure in the females that is unique to this insect group. This structure helps to protect them from the onslaught of bacteria and other nasty material that is introduced into the female's body with the sperm. The bugs seem to be unable to distinguish males from females until rather far along in this process, which means that a certain proportion of the time, males will attempt to mate with other males. Bat bug males, it turns out, also have structures at the wound site that are similar to those possessed by females, although these differ in some anatomical details. Scientists from the University of Sheffield in the United Kingdom who study the insects speculate that the males evolved these structures to signal other males that they are not females, and perhaps even to provide some protection from pathogens in the event that the male doesn't get the message. Here too, selection on males to be profligate with their mating attempts may simply have overruled selection to be more reserved, even with some unwanted side effects.

So a certain amount of homosexual behavior isn't any more of a mistake in the beetles than any other trade-off between two traits might be. Instead, that very flexibility in mating behavior, where decisions are made based on shifting criteria that may be apparent only at the last moment, might itself be favored by natural selection. It allows animals to be opportunistic in their behavior, and increases their ability to roll with the punches of a changing environment.

Mistaken identity, however, doesn't seem to be what's going on in a tiny fly that lives on the water lilies of English streams. Males wander on the surface of the leaves, pouncing on anything that remotely resembles a female and a few things that do not, such as gray specks of decay on the plants, or flies of other species. After he succeeds in mounting a female, the pair embarks on an elaborate courtship ritual in which they rock back and forth for up to 15 minutes. An uncooperative female quickly puts a stop to this activity, in which case the male leaves without bothering her further. Sometimes, however, a male mounts another male, and in these cases the mounted individual vigorously resists the overtures while the mounting male clings to his back as if to a tiny bucking bronco. Ken Preston-Mafham, who has studied the flies in War-wickshire, believes that the mounting male is preventing his partner from getting to the females that will light upon the lily leaf. If males are competing for access to the females, a male that simply rides another individual is in the best position to leap off his rival and seize the female himself.

Finally, there may be some unforeseen advantages to homo sexual behavior, regardless of why and how it arose. As I mentioned, flour beetles, the tiny pests infesting your kitchen cabinets, are useful models for genetic and other biological research. Like the other insects I just described, male flour beetles will mate with other males. Work in Sara Lewis's laboratory at Tufts University in Massachusetts showed that when one of the males mated with a female right after such a homosexual interaction, on a few occasions enough sperm from the other male was left that it actually fertilized some of the female's eggs. Although this is unlikely to be a frequent occurrence, it suggests that some reproductive benefit could partially offset any wasted time or effort in the male-male interactions.

Flies with Designer Gay Genes

WEIRD sexual proclivities of bedbugs aside, what people really want to know is whether homosexuality has a genetic basis. Because it is much easier to search for such genes using quick-breeding study animals, the fruit fly Drosophila has become the poster insect for studies of sexual orientation genetics, as it has for so many other traits. Although people rarely identify with insects, particularly tiny buzzy ones such as flies, in this case the media has reliably been all over any new finding that deals with homosexuality in Drosophila, with headlines such as "Fruitflies Tap in to Their Gay Side," "Gay Drunk Fruit Flies," and even "Gay Fruit Fly for President" (not sure what that was about, frankly). Google "gay fruit flies" and you get upward of 270,000 hits.

Scientists were not looking for homosexual flies when they began this research. Indeed, most if not all of the researchers whose papers end up providing fodder for headlines like those above would not describe themselves as studying sexual orientation at all. Instead, they are trying to understand how the brain sends and receives signals from the sense organs, or attempting to break down the processes of courtship and mating into their most fundamental components. What exactly has to happen for boy to meet girl so that baby can make three (or thirty, or maybe three hundred, in the case of the flies)?

It turns out that sex, even for such relatively simple animals, requires a sophisticated orchestration of steps. Although different species of Drosophila do things somewhat differently, in many fruit flies the females must go to a specific kind of rotting fruit or other plant matter to lay their eggs. When they are there, the males detect the presence of a potential mate by smelling the surface chemicals on the female's body, and then pursue the object of their affection, performing a stereotyped series of movements, attempting to lick the female, and vibrating their wings to produce a song that is audible to human ears only if it is greatly amplified. The details of the movements and the song vary among species, and males differ in how vigorously they perform the actions and in the way in which their advances are received. Often the female walks away or lashes out with her legs in response. If a male is successful, the female stops long enough to allow him to mount her and transfer his sperm. Both in the laboratory and in the wild, males will also attempt to court other males, particularly younger ones that have just become adult.

One can, of course, study the flies simply by observing their behavior using a magnifying glass to get at some of the finer details, but for many years scientists have been using extremely sophisticated genetic technology to understand exactly which genes control which aspect of the mating ritual, and how they interact. It is now possible to produce knockout strains of the flies, which lack a particular gene but are otherwise like normal, or wild-type, as they are called, Drosophila. Alternatively, scientists can manipulate individual genes so that they are still present but are inactivated; genes can also be inserted into places they wouldn't normally occur.

One of the most important genes regulating sexual behavior in the flies is called fruitless (many genes in model organisms have special names, some of which are quite fanciful, for example, sonic hedgehog). Flies with one kind of mutation in this gene will try to court females, but they do so incorrectly. It's still not clear where their problem lies, but it may be that they fail to fully extend their wings to sing, a deal breaker from the female's perspective. This defect applies only to courtship—the mutants can fly normally and can flick their wings dismissively when rejecting advances made by another male. Flies with other types of mutations of the fruitless gene court both males and females. When several of the mutant males are placed in a Petri dish, they form male-male courtship chains in which each male is simultaneously both courting and being courted. Female flies with the altered fruitless gene will court other females with the same stereotyped set of movements ordinarily used by males.

The fruitless gene affects many different parts of the fly brain, each of which is important in regulating sexual behavior. A Japanese researcher, Ken-Ichi Kimura, meticulously dissected the brains of Drosophila that did and did not have the mutation in fruitless. He and his coworkers found that a just a handful of nerve cells in the wild-type males are absent in the males with the mutation. In the females that court other females, the cluster is also present, although normal females lack it.

So is fruitless "the gay gene," or do the nerve cells themselves keep flies from being gay? Not so fast. Kimura and his colleagues also worked with mutations on another gene, called doublesex. They found that a nerve cell group that is affected by mutations on both of the genes simultaneously can turn on courtship behavior in females. Ordinarily, this cell cluster dies in females because of a feminizing protein in the brain, but if fruitless is present, the cluster survives. Both of the genes are needed to ensure that males court females and females don't.

Then are both genes "gay genes"? Once again, no. Just having the genes that control the courtship behavior itself isn't enough. A male also needs to distinguish that a female is out there in the first place, which means processing the sight, smell, and maybe sound of another fly, and yet more genes seem to be involved in that process. The male flies' behavior is triggered by pheromones, or odors that are emitted by the female. Females that have already mated, and hence are more likely to reject the courtship advances of subsequent males, produce a different odor than virgin females or other males. But the male also needs a gene to enable him to detect those chemicals. Flies don't have separate taste and smell organs; they detect both with sensory cells on their feet (which is why they often walk on things before deciding whether they are food, and why they can spread germs so easily), and work by researchers at Duke University published in 2008 showed that a pheromone detection gene was critical to the mating game. This one is unimaginatively dubbed Gr68a, and males with a mutation in it will court already-mated females as well as other males, and they will even go beyond the tapping and singing behavior to try and actually mate with the males. What is more, the signals that it receives bypass the rest of the nervous system and go directly to the brain. Such an express route is unusual for a smell or taste receptor, which underlines the essential nature of Gr68a to the mating process.

Other flies that exhibit male-male courtship have alterations in genes called dissatisfaction, prospero, and quick-to-court. What's more, the neurochemical dopamine, which is important in a wide variety of physiological activities, including learning, movement, and the brain's processing of painful or pleasurable stimuli, also turns out to feature in same-sex courtship in Drosophila. Dopamine is found in many animals, both vertebrate and invertebrate, including humans, but if you increase it in the flies, males are more likely to court other males, although they don't change how they react to virgin females or to odor cues in general. And if news about dopamine alone leaves you cold, further research in this area demonstrated that when flies genetically altered to be unable to release dopamine at normal temperature were exposed to ethanol, the type of alcohol in beer, vodka, and other adult beverages, they too exhibited same-sex courtship. The male-male courtship became more pronounced with repeated exposure to the alcohol; the experimental arena where the scientists placed the flies was quickly named the "Flypub," and the inevitable news coverage trumpeted, "Fruit Flies Prove That Alcohol Makes People Gay."

Better Sex through Chemistry

MOST of this research used flies that exhibited the altered behavior permanently. But one of the most exciting new developments in the genetics of Drosophila sexual behavior showed that the tendency to court males or females could be switched on or off within minutes.

Dave Featherstone at the University of Illinois in Chicago said in an email to me that he was envious of what I do, because he "got into biology because I imagined myself traveling all over the world living in the wilds watching animals. Somehow I ended up studying bizarre minutia in a lab. I might as well be an accountant." As someone who does watch animals in nature for a living, at least some of the time, I was flattered by his comment, but his modesty underplays the significance of his work, which is hardly bizarre or trivial. Featherstone is interested in how the cells of the nervous system send and receive messages, particularly across the gaps between them, called synapses. His laboratory focuses on a nervous system chemical called glutamate, which his website describes as follows: "Glutamate is the voice by which brain cells speak to each other. Glutamate receptors are the ears by which they hear."

Information—whether about sex, food, or anything else—does not simply slosh from one nerve cell to another, making its way haphazardly to the brain. Instead, the receptors regulate which memories are retained, which behaviors are executed, and which signals are recognized as important. So Featherstone studies glutamate and its role in brain messages using Drosophila, which show many of the same patterns of glutamate use as humans but are obviously much easier to manipulate.

For the work on the chemical courtship switch, Featherstone and his colleagues used male flies with a form of yet another gene called genderblind. Males with a mutation of that gene, like the fruitless mutants, will court other males as well as females. This is simple observation—what is exciting is that the scientists went on to pin down why. The genderblind gene controls the transport of glutamate out of glial cells, which are nervous system cells that do not conduct electrical signals themselves but communicate with and support other cells. Glutamate in turn can control the synapses, those junctions between other nerve cells, and synapse strength is important in determining many aspects of behavior. By altering synapse strength either genetically or chemically, independent of the mutation, the researchers could alter, sometimes within minutes, whether the flies would court males as well as females, or only females. Then they could be switched back again. The altered males interpreted the pheromones of other flies differently than their wild counterparts because they had too many glutamate receptors at the junctions between the nerve cells. What would ordinarily be a male smell that induced other males to keep away was perceived by the mutants as stimulating.

What exactly was going on? Recall that even wild-type male Drosophila will court other males, particularly when they have recently become sexually mature. The courted males reject them, and they learn to stop trying, generally within about half an hour of getting nowhere. But the genderblind flies just don't take no for an answer, which suggested to Featherstone that what was really happening was at least partly a failure to learn from experience. Current research in his lab is focusing on how glutamate is involved in this learning process. Ironically, then, the search to find genes and chemicals associated with courtship and mating led to the discovery that learning, that most plastic of behaviors, is at the heart of the matter. Nothing could be farther from demonstrating that a gene or genes causes homosexuality.

Regardless, the media fell on Featherstone's discovery like gay-gene-seeking jackals. Perhaps because of the rapidity of the switch, commentators seemed to think that the work indicated it was possible, even likely, that scientists could develop a pill that would alter human sexual orientation, and hence be used to "cure" homosexuality, or that said drug could be used recreationally, so that one could be gay under some circumstances and straight under others. When I wrote a brief op-ed piece about Featherstone's work for the Los Angeles Times, in which I noted that the really interesting part of the research, the role of glutamate, had gotten ignored in all the brouhaha, I got emails accusing me of promoting genocide of homosexuals. Another article's title demanded, "If There Was a Gay-Straight Switch, Would You Switch?" Never mind that not a single answer to the question appeared in the article itself. Even some of Featherstone's colleagues questioned his use of the word homosexual in his paper on the work, calling it "tabloid language."

Aside from the fact that anyone who thinks that "homosexual" is tabloid language hasn't been spending nearly enough time at the grocery store checkout, much of this reaction was seriously off base. Featherstone points out that his work looked at courtship behavior that was indeed directed at members of the same sex, hence homosexual. But many people use the word to talk about sexual orientation, or the preference for one kind of partner over another. As he says, "Our data as well as recent data from mice suggest that mate choice is not some sort of 'compass arrow' that can only point at one target.... Let me make an analogy: mate choice is a lot like food choice. The fact that I like corn dogs doesn't keep me from liking pizza. They are separate sets of sensory stimuli, to which I can respond independently.... 'Homosexual' and 'heterosexual' are simply descriptive terms that define particular types of mate choice, same as 'corn dog' and 'pizza' define particular types of food."

This still doesn't suggest that in humans, sexual preferences are as easily manipulated, or that we become gay or straight with the same facility with which we choose our lunch menu. (Though, really, Dave—corn dogs?) But it does illustrate how easy it is to have this research misinterpreted by scientists and nonscientists alike.

Taking a Pill?

SO WHAT does the research from insects tell us about homosexuality? All of the scientists using genetic alterations in Drosophila hasten to point out that despite the flies sharing 75 percent of human disease genes, no counterpart to fruitless exists in people. So even though what the flies are doing looks at least somewhat like what humans do, the insects got to a similar destination through vastly different modes of transportation on different highways.

It is certainly true that the attraction to members of one's own sex is common in nature among many species, and its sources can be traced in the lab, at least for the flies. If that resonates with your world view on homosexuality, whether to accept or eschew it, so be it. But homosexual behavior means something different to the flies than it does to more complex and more social animals, such as the primates, birds, and other vertebrates that exhibit same-sex behavior. For example, Laysan albatross in Hawaii form female-female pairs that stay together for many breeding seasons, rearing chicks together if one or both of them has been inseminated by a male in the colony. Bonobos, smaller relatives of the chimpanzee, frequently exhibit sexual behavior between males or between females; sex seems to be used in bonobo society as a way to resolve social tension in the group. In these and many other animals, sexual behavior is about more than reproduction. People unfamiliar with life in the wild often envision animals keeping their sexual contact to a businesslike procreative minimum, where male and female meet, mate, and part as soon as the plumbing has everything lined up. But in social animals, sex is not just reproduction—it is communication, part of a continuum of dealing with other members of your species.

Fruit flies and the other insects I have been discussing do not have elaborate social systems in which such subtleties are important. Yet they still exhibit same-sex courtship and even mating. The conclusion, though, is not that bugs are stupid, but that sex is hard. Figuring out how to do it involves a complex interplay between genes and the environment. Featherstone and many of the other researchers using genetically modified flies measure their behavior by observing how the mutants respond, not to a living, breathing companion, but to a male or female with its head cut off. The fly's body still emits the same odor cues and provides the same audience for the displays, but it obviously cannot interact with its partner. The decapitation controls for the inevitable interaction between individuals that could alter the results. The genes don't just issue commands that make the flies behave in a certain zombielike way regardless of circumstances. Instead, the genes, and the chemicals they deploy, affect the way that experiences such as being rejected or accepted by another fly are interpreted.

The flies and other insects may also use some of the same-sex interactions as a way to practice their technique. Young male Drosophila are often courted by older ones, and Scott McRobert and Laurie Tompkins showed that males that had been the recipient of such courtship in the lab were more successful in wooing females later in life. The difference was not huge, but in evolution, every little bit counts. In a different species of Drosophila than the one used for most of the genetic research described above, males that are isolated from other flies during development have a hard time telling their own species from similar ones, a crucial skill, since hybrid offspring are not fertile and, hence, an evolutionary disaster. It takes experience with one to know one, it seems, even though Drosophila lack a true social organization like that of wolves, bonobos, or even bees. These flies also exhibit male-male courtship, with the socially ignorant males showing it much more frequently than males reared in the company of other flies.

Part of what seemed to get the public so excited about Featherstone's work was the idea that it wasn't a gene, but "a chemical" that altered the sexual behavior of the flies, which led to the speculation about popping a pill to change one's sexual orientation. If what's sauce for the fly is sauce for the human, this could mean that chemicals in our own nervous systems are involved with sexual orientation, too. But I don't find this in the least alarming, or indicative of some dystopian possibility of transforming people from gay to straight and back again. The truth is that chemicals no more control who we are sexually attracted to than they do anything else. Which is to say, everything and nothing.

Chemicals are where the body's rubber meets its road. They are how our genes exert their influence. It's fine to say that a gene controls eye color, or digestive speed, or whether we like mangoes, but what does that mean? Somewhere, a chemical is involved. Better living through chemistry? It's more like living through chemistry, period. Featherstone's lab has winkled the details out of the devil by connecting the gene to the proteins it codes for and the action of the substances those proteins control. None of that alters the crucial role of experience, even in a creature such as the fruit fly.

What does Featherstone himself want to do with this information? He doesn't seem motivated to get in the pocket of Big Pharma and develop a drug to enable people to go from straight to gay. Presumably he recognizes that this isn't possible. But he has some ideas. Going back to his website, "An understanding of Drosophila neuroscience raises the possibility that we may be able to engineer a ruthless bionic insect army, and use it to take over the world. From our despotic biotechnological throne, we can seek revenge on everyone who ever wronged us. What's that? A buzzing in your ear? I hope you're on OUR side."

All I can say is that I assume he is saying this with tongue in cheek. I really do.