Sex on Six Legs Page 13

  Some recent work by Luke Holman and Rhonda Snook at the University of Sheffield in the United Kingdom suggests that looking at the situation from a female perspective may help explain the evolution of this obviously masculine trait. They used yet another species of Drosophila, D. pseudoobscura, which also has the two sperm types, to see whether female flies might be the ones controlling the situation. Indeed, many of the sperm are actually killed by the chemicals or cells present in the female's reproductive tract, and the DNA-containing eusperm seem to be particularly sensitive. When males produced more of the parasperm, the eusperm were protected from the spermicidal activity. The parasperm appeared to be acting as shields for their more fertile brothers. A few authors actually refer to the parasperm as soldier sperm, but I think that presumes that they are fighting each other, when as Holman and Snook point out, the female seems to be playing an active role in their demise.

  Why should the female reproductive tract be such an unwelcoming environment for sperm? Holman and Snook speculate that one possibility is that females are using their own reproductive organs as a screening device, making the sperm from various males run (or swim) a gauntlet of tests before being allowed to fertilize the eggs. In other words, cryptic female choice could explain the evolution of a seemingly nonfunctional cell type. The criteria that the females might use to distinguish among suitors are not well understood. It may be that, as with the exceptionally long tails of the giant sperm in D. bifurca, parasperm are a kind of secondary sexual trait, like the peacock tail.

  An answer to the question of why sperm are so variable, as well as how likely it is for females to sort through sperm in their reproductive tracts and the function of all those chemicals in the semen, will likely require examining the situation from the sides of both males and females. The fierce activity that occurs inside a female after copulation does, however, provide a possible insight into that sex difference in postcoital behavior. With all that commotion going on in there, who could sleep?

  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, particu
larly 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 (Amphipyra spp.) 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.