The surprisingly gay world of insect sex

Homosexual behavior isn't just a vertebrate thing. But what can bugs teach us about our own sexuality?

Published August 21, 2011 2:01PM (EDT)

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 online debates.

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!"

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.

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."

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.

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 Warwickshire, 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.

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.

Because it is much easier to search for the genes responsible for behavior 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.

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 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. 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."

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.

Marlene Zuk is a professor at the University of California, Riverside. Her books include "Sexual Selections: What We Can and Can't Learn About Sex from Animals" and "Riddled with Life: Friendly Worms, Ladybug Sex, and the Parasites That Make Us Who We Are."

Excerpted from Sex on Six Legs: Lessons on Life, Love and Language From the Insect World by Marlene Zuk, copyright © 2011. Reprinted by permission of Houghton Mifflin Harcourt Publishing Company. All rights reserved.

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