I hold the dubious distinction of being something of an expert on the sexual behavior of houseflies. This is not due to some bizarre fetish or fascination with fly sex. Rather, I became the resident brain on the ins and outs of the reproductive habits of Musca domestica because my boss told me to.
It was 2005, and I’d been working for Drion Boucias, head of the Insect Pathology Lab at the University of Florida, for a year when he suggested I run a full-fledged experiment, a step up from my usual undergrad lab duties of scrubbing beakers and counting beet armyworm moth eggs. Drion was a sharp and thorough scientist, old school in his zeal for research. He’d also biked to work in his boxers once and puttered around the lab until someone told him he’d left his pants at home. He was both intimidating and encouraging to students, and while he often reminded me he could hire a convict to do my job for less, he never did.
When he asked what insects I liked working with, I told him I was game for anything. “I’m not too hot on maggots or cockroaches though,” I said.
He decided to set me up with houseflies. Houseflies, I knew, were not only uninteresting but were also nothing more than adult maggots. I kept my mouth shut. It was the start of my senior year, and I had thirty dollars to my name. Plus, I was an English major and lucky to be in the lab in the first place. An entomology minor, afraid of the two years of chemistry, physics, and other weed-out classes the major then required, I’d impressed Drion with my writing in his “Principles of Entomology” class, but I knew he could have taken on any number of science students in my stead.
So, when he dispatched me down the road to the U.S. Department of Agriculture’s Center for Medical, Agricultural, and Veterinary Entomology to learn how to rear flies from their fly guy, I hustled.
The fly guy at the USDA was a grad student from Argentina with a backward baseball cap and a belly I found attractive. He gave me a tour of the fly-rearing facility, opening one of the large walk-in incubators that housed the many colonies.
“You want to keep it humid,” he instructed. “And simulate the natural cycle: twelve hours of light, twelve hours of darkness.”
The larvae were kept in deep trays of compost material stacked on the wheeled racks typically found in cafeterias. He pulled one out and turned the dirt over with a bare hand to expose a mass of maggots. “Here are the little guys. You don’t even need to cover the trays—they can’t climb out.”
I looked down at thousands of wriggling bodies: blind, limbless, and with those two tiny hooks at the end of what would be, in another animal, the head. They were the elephant seals of the insect world. Unforgivably ugly.
The fly guy gave me a box of pupae to start. The pupae—the life stage between larva and adult—were much easier on the eyes; the repulsive forms of the maggots were hidden inside clean, brown shells with neatly spaced striations. When I shook the container, it made a heavy sound, like a box of beads. I biked back to the lab, clutching the colony against my handlebars.
• • •
In the early nineties, Drion was part of a research group that discovered a naturally occurring disease in populations of wild houseflies in the dairies of north Florida. Known as Musca domestica salivary gland hypertrophy virus, or MdSGHV, the virus causes severe hyperplasia of a fly’s salivary glands, meaning the glands swell enormously. Sometimes they grow so large they coil and contort over themselves to fill most of the fly’s body cavity. In the worst cases of infection, the virus can inhibit feeding altogether, starving the fly to death. However, this is quite rare; the virus has developed the ability to replicate exponentially in the glands of an infected fly without killing its host. Keeping a fly alive is extraordinarily beneficial to the virus, particularly as its main means of transmission is per os, that is, by mouth. MdSGHV-carrying flies can contaminate whatever surface they feed on, and only one droplet of saliva is needed to trigger the complete infection of another fly.
After publishing a description of the virus, Drion’s lab had moved on to other diseases, not seeing any profit in pursuing MdSGHV further. But with my work-study labor at his disposal, Drion decided to return to his study of the virus, focusing on other possible means of transmission. Specifically, he wanted me to conduct an experiment that would either confirm or rule out the possibility that it could be passed sexually and/or vertically—from infected parent to progeny.
While houseflies don’t directly vector diseases through a bite, as many other insects do, they can mechanically transmit pathogens that cause illnesses such as salmonella poisoning and dysentery. And they can be a nuisance, especially in dairies, where fly populations can reach plague-like proportions. Since MdSGHV is a disease that can’t be transmitted to mammals or humans, Drion was interested in the possibility of using the disease as a biological control of flies, a novel concept as most other controls target the immature life stages of the fly, not the adults.
• • •
Salivary glands are crucial to a fly because of their role in digestion. The housefly cannot chew. If you look a housefly in the face, under its eyes, you’ll see a tubelike appendage that can be extended and retracted like an arm. This is the proboscis, which functions much in the same way as a giant straw. At the end are two large fleshy lobes lined with bristle-like hairs, the labellum. When a fly lands on a potential source of food, it tastes it with sensors in its labellum and on its leg hairs. If it likes what it has found, the fly will regurgitate digestive enzymes from its salivary glands onto the dish. The enzymes get to work, breaking down the food into a hearty liquid form. The fly then uses its mouthparts as part-straw, part-sponge to slurp up the broth.
It’s not just your food that is in danger of being puked on by a fly, though. Houseflies are like babies—they’re compelled to taste everything they encounter.
In the early days of the experiment, it was difficult not to jerk my hand out of the cages when the flies landed on me, as they invariably did. But I grew accustomed to their touch, even when I could feel dozens of tiny, moist labellum daub at my arm, sampling the flavor of my skin.
• • •
Verena, Drion’s tall German colleague and my immediate supervisor, showed me how to dissect out the salivary glands from an infected fly and prepare them into a filtrate that could be injected into healthy flies. MdSGHV not only resulted in hypertrophied glands, but also turned them an outlandish blue, the kind of color you would only expect to find in deep-sea creatures. It was actually quite beautiful.
Drion often grilled me, looming over my shoulder as I injected unconscious flies, the needle making a startlingly large hole in the thorax. How many days until the pupae hatched? How long until the adult flies were sexually mature? What did they need to eat?
“Read up,” he told me. “I want you to be able to answer any question I throw at you.”
But literature on the life cycle and behavior of houseflies was surprisingly scarce, and the research I managed to dig up was usually dated from the seventies. Most of the present-day articles were highly specialized, focusing on aspects of genetics and biochemistry, with titles like “Mass spectrometric analysis of putative capa-gene products in Musca domestica and Neobellieria bullata.”
I asked Verena about the knowledge gap.
“It’s not popular to study insect behavior anymore,” she said with a measure of regret. “It’s seen as kindergartner stuff—not ‘scientific’ enough.”
In other words, anybody could watch bugs.
That was how I got into entomology in the first place. A fanatic about animals from my earliest years, I collected and studied insects and arachnids as a kid when more traditional pets were lacking. Some of my earliest memories are of talking to two large spiders that lived in a bottom bookshelf—and weeping when one fell victim to the vacuum cleaner. In elementary school, I caught crickets and kept them in an empty coffee can outfitted with crumpled paper towels, sticks, and tiny trapezes made out of paper clips. I wrote a three-page instruction manual for other would-be cricketeers, which included a note that if you forgot to feed them, they would eat each other.
In college, I could be found getting a leg up to net a praying mantis at my dorm light or stuffing the freezer with bags and jars of specimens to my roommates’ chagrin. I felt flattered when a friend told me, “I saw a weird bug the other day and thought of you.”
• • •
The paucity of publications on normal housefly behavior meant that I had to spend a lot of time observing the habits of healthy flies and then verifying what I saw in old articles. Sometimes, the results astonished me.
Take the sex.
Previous research had prepared me for some of what transpired when I combined healthy virgin male and female flies in a mating cage (the cage is less exciting than it sounds, consisting of a plastic container with a cotton sleeve over the mouth). As soon as the flies awoke from their cold-induced slumber, the males started “striking” the females. The strike is like a gentle pounce. The smaller male lands on a resting female’s back and crouches near her head. Using his forelegs, he strokes her head several times; then he shuffles back and curls his abdomen under hers. All this had been well documented, but when I strained to see the finer details of copulation, what I saw caught me off guard. I waited until I had observed the phenomenon in more than one couple before I called Verena over to take a look.
“Is it just me,” I said, “or is the female penetrating the male?”
She adjusted her glasses and peered into the mating arena. “Hmm. That is interesting.”
In insects, the male sex organ is known as the aedeagus, and in houseflies, this is visible at the end of the abdomen as a dark round stump. The genitalia of the female housefly, in contrast, is a needle-like ovipositor, which is normally withdrawn into the abdomen but can extend like a telescope during intercourse and when laying eggs. A female generally mates only once during her lifetime; after insemination, she stores the sperm in organs called spermathecae, allowing her to fertilize her own eggs, laying them in daily batches for about a week.
What we had presumed about housefly copulation was that the male inserted his aedeagus into the female sex organ and deposited his sperm. However, as we watched, we realized that it was the female who responded to the male’s courtship ritual by extending her ovipositor into his genitalia. Essentially, she controlled the mating; she collected the sperm for herself. This explained all the preliminary fussing and foreplay. It’s impossible for a male fly to force himself onto or into a female. All he can do is feel her up, shimmy back to her abdomen, and wait.
Even more surprising than the mechanics of housefly sex, though, was the virtual absence of any mention of it in publications. Scouring articles, I only found two lines in the introduction to a decades-old source that acknowledged who was penetrating whom. With more of the literature online now than in 2005, I’ve seen a few other articles that note the female fly’s unusual agency, but these, too, are older studies. To the larger scientific community, this role reversal seemed long forgotten.
Another fascinating feature of housefly sexuality is the male’s rapacious sexual appetite. Unlike the female fly’s monogamous lifestyle, the male spends his ephemeral adult life trying to inseminate as many females as possible. In publications, his desire to copulate is often described as “avid.” Even males who have just finished copulating for eighty minutes—houseflies generally mate for an hour or more—will hop back onto the female, who, by that point, has all the sperm she will ever need and placidly ignores his love-pats.
In the absence of responsive females, males will attempt to mate with flies of different species, other male flies, and inanimate objects. I witnessed a male fly desperately trying to mate with a pebble, lavishing caresses on it and waiting in vain for it to respond. Verena and I theorized on how the males could be so, well, stupid.
“He has to know it’s not a female, right?” I said. “It doesn’t smell like one, look like one, or even feel like one.”
But what happened when the males were unable to satisfy their lust was both funny and tragic: they would literally drive themselves insane. Consumed by the urge to procreate, male flies that were kept from females would rocket out of control, flying headlong into the walls of their cage until they destroyed their wings and lay at the bottom, spinning madly on their backs. Eventually, they lost all will to live. If I took out a cage of virgin males that had been left alone for too long, I would find hundreds of dead flies in a furry heap, their wings ripped to shreds, the fresh water and food left untouched.
• • •
Verena and I poked fun at the self-destructive males, but secretly, I empathized with them.
I knew exactly how they felt. I practiced celibacy for religious reasons—maybe endured is a better word. Many days, I was dizzy with desire, locked in contention with my body, unable to think clearly as I biked to the lab, my eyes resting briefly on every man I passed.
My only brush with romance that year was with a contemplative, cultured graduate student who shared my faith. After a couple of dates, I backed out, confessing a lack of attraction. He chided me in an email for thinking love required some kind of physical click and suggested I read a Wendell Berry essay on marriage to amend my views. I laughed, shook my head, and sent no reply. But for a long time afterward, whenever I thought of his words, my cheeks burned with anger and, for a reason I could not explain, shame.
• • •
Because much of the experiment revolved around different combinations of couples—healthy female/infected male, infected female/healthy male—I had to ensure that the females were virgins. The only way to do that was to segregate the flies according to sex as soon as they hatched out of their pupal cases. There was urgency to this; if I waited too long, the males would mate with every female they could get their hind legs around, rendering those females indifferent to the males in the mating cages and warping the data.
After knocking out the newly emerged flies by putting them in a freezer for a few minutes, I placed them in plastic trays on ice on a lab bench, plucking out the males and dropping them into a separate container. Abdomen up, the size of the genitalia told me the sex. Abdomen down, the eyes would give it away: females’ eyes are fully separated while males’ eyes almost touch at the top of their heads, tilting downward like an upside-down “v.”
The flies would begin to stir and twitch after just a few minutes under my breath, but I could not afford to make a mistake. Just one overlooked male could wreak havoc on a population of virgin females.
During the trials in which the males were infected with the virus, the males continued to mate even when their salivary glands were so bloated they could hardly fly.
In the infected female/healthy male combination, the results were more surprising. The infected females were still attractive to the males, who would approach their potential mates with confidence, stroke their heads, and scoot into position for a good old-fashioned copulation. But the males’ efforts went unrewarded. The infected females flat out refused to mate, though they otherwise demonstrated completely normal behavior.
At first, the males were patient. When a female did not extend her ovipositor, the male would climb back up to her head, stroke her again, and wait. This could happen several times before he reluctantly gave up, flying off in pursuit of a different mate. But none of the other females were having it either; they were all stubbornly unmoved by the foreplay.
I dashed in to Drion’s office with the news: “They’re not mating!”
But Drion didn’t share my enthusiasm, pointing out the possibility that the females had been inseminated on the sly. “Maybe some male is having a heyday in the females’ cage. Are you sure you didn’t screw things up?”
I wasn’t. So, after several hours in which the frustrated males tried again and again to coax an ovipositor out of an unresponsive infected female, I froze them and dissected the females to ensure they had not already been inseminated. The female housefly has three spermathecae, each the shape and color of a walnut. These organs store the sperm, releasing them as eggs funnel down from the ovaries, en route to the ovipositor. Carefully, I removed the spermathecae, mounted them on a slide, crushed them in saline, and took a look underneath the electron microscope that was—as Drion regularly told me—worth more than my life. I searched for the clear, spaghetti-like strands of sperm. Nothing.
“Run the experiment again,” Drion said.
I reared, sexed, and infected another batch of flies, and placed them in the mating cages. Again, the males were still attracted to the infected females, and again, their efforts were rejected. Within a few hours, the males started hurling their bodies against the sides of the container, some beating themselves to death. Meanwhile, the females ran their forelegs over their heads and bristles leisurely, and sipped at the water supply, balancing on the Styrofoam chips that kept them from falling in and drowning themselves.
• • •
The implications of our mating experiment were that the MdSGHV virus either caused sterility in females or rendered them unresponsive to potential mates. No mating meant no maggots, and no maggots meant no adult flies. The presence of the virus, therefore, could significantly curtail housefly populations. The lab published a successful article on the results, proposed a new group of viruses, and got a grant to boot.
When I graduated in 2006, the research was still on, and Verena and Drion were floating ideas on how the virus could be made into a commercially available pesticide. Importantly, a sister lab in Kenya, working with a closely related virus, found that it causes sterility in the bloodsucking tsetse fly, the vector of the often fatal trypanosomiasis, or “sleeping sickness.”
More recent research has revealed how the virus puts the kibosh on fly sex: in houseflies, MdSGHV can curb egg development in females. In tsetse flies, it causes the female reproductive organs known as ovarioles to develop irregularly and can halt the male flies’ sperm production. Infected male tsetse flies are often incapable of inseminating females.
What remains for me are the story and party trick of being able to discern a fly’s sex at a glance. I’m not sentimental about houseflies even though I adhered to their pace of life for a year, structuring my schedule around the stages of their morphological and sexual development, telling friends I would be at the bar as soon as I had sexed the flies. I could not escape them even in my dreams.
Do I own a fly swatter? Yes, but I don’t always use it. Either way, I always pause to look at the fly sponging at an apple on my kitchen table or cleaning itself like a cat. I note the distance between its eyes, the buttercup color of its abdomen, and think, “I know you right down to your ovaries.” Then she’s gone.