Sex on Six Legs Read online

  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.