Zoobiquity

  Hydrophobia, or fear of water, is a classic symptom of rabies infection. So is aerophobia (fear of moving air) and, as the disease progresses, an uncontrollable urge to bite. These seemingly random behaviors stem from changes the virus causes in the central nervous system of its host. And they may have a fortuitous side effect for the virus itself. The actions may actually help it transmit itself into a new victim. Because the rabies virus is spread through saliva, causing an urge to bite, for example, would be a useful microbial “strategy.” So far, however, infectious disease veterinarians haven’t found adaptive purposes for causing a fear of water or moving air.

  Or consider Enterobius vermicularis, a.k.a. pinworms. This common childhood infection alters human behavior by drawing hands away from more productive activities, like homework and setting the table, and redirects them into ferocious anal scratching. This scratching serves two purposes for E. vermicularis: It helps burst the gravid females’ bodies, releasing the ten thousand eggs they each carry. And it helps those freshly exposed eggs burrow under the child’s fingernails, where they wait patiently for the next thumb suck or nail bite to permit them entry into the host’s mouth and, from there, his GI tract, where they reproduce.

  Or take Toxoplasma gondii. Infection with this protozoan has an unusual effect on rodents: it makes them lose their fear of cats. From the rodent’s perspective, of course, this is terrible. It makes them easy prey. But from the toxo’s point of view, it could not be more clever. That’s because the only place on Earth that Toxoplasma gondii can reproduce is inside a cat’s intestine. By making rodents fearless, the parasite practically gift-wraps and delivers itself to the cats’ claws and jaws … and from there to guaranteed reproduction.

  Humans are “dead-end” hosts for toxo, meaning it can’t reproduce in us. But the parasites can still enter our bodies when we eat or touch infected meat, soil, or cat feces. Once inside our brains, the toxo can “encyst,” essentially lying dormant and waiting to get back into a cat. The pathogen doesn’t know whether it’s in a mouse or a mail carrier, a rat or a receptionist. But it continues to produce chemicals and help itself to nutrients in our blood and tissues. In fact, many of us have these encysted toxo infections. And, incredibly, this microorganism may affect our behavior as individuals. Exposure to toxo in the womb may be a contributing factor in developing the often devastating human disease of schizophrenia.

  “Brainworms” and other parasites have been shown to spark killing sprees within ant colonies and make crickets and grasshoppers suicidal. One wasp creates a bodyguard for its offspring by infecting a hapless caterpillar which then fights off the wasp’s stinkbug predators with powerful swings of its caterpillar head. While toxo, pinworms, and rabies aren’t STDs, certain sexually spread ailments work their own microbial puppetry on their hosts. Two STDs—HIV and syphilis—notoriously produce extreme behaviors in people with end-stage infections. HIV dementia compromises judgment and memory. The egomania, impulsivity, and disinhibition that characterize advanced syphilis may have not only propelled the infamous sexual appetites of known syphilitics Al Capone, Napoleon Bonaparte, and Idi Amin but facilitated their power grabs as well. And while patients in the late stages of syphilis are no longer contagious and can’t spread the disease, there are diseases where the behavior caused will promote infection.

  And this is another way we can learn from animal STDs. Many microbes depend on sex for their transmission. It makes sense that they might induce subtle sex-friendly behaviors, if they could.

  But how would a crafty STD microbe get people jumping into the sack with each other? Maybe it would improve the males’ pickup lines … or confuse normal signaling so that rejections got misinterpreted as come-ons. Maybe it would make the females more alluring. Or increase libido or lower inhibitions to lead to more sex.

  This may indeed be exactly what goes on in a range of animals infected by STDs. Male Gryllodes sigillatus crickets attract females with intricate symphonies of sound, produced by rubbing their hind legs together. Crickets infected with a certain parasite sing slightly differently than uninfected crickets—but the change seems to increase the males’ attractiveness and bring more females their way.

  When infected with the sexually transmitted virus Hz-2V, female corn earworm moths start producing excessive amounts of sex pheromones—some two to three times as much as their uninfected sisters and peers. The extra come-hither perfume is believed to attract more male moths—thus aiding the spread of the virus. Intriguingly, these infected females also demonstrate a kind of lepidopteral “no means yes” behavior. Apparently unaware of how politically incorrect it is, they appear to further excite their mates through acts of resistance.

  Sexually acquired infection can spur some animals into assertive sex-seeking behaviors. Male swamp milkweed beetles infected with a sexually transmitted mite aggressively move in on nearby mating pairs, busting up the action and pushing aside the other male. When no females are in the vicinity, these infected males approach and attempt to mate with other males.

  STDs may even change the “behavior” of plants. Like all living things, plants need to reproduce. For flowering plants, this means getting the sperm-laden pollen from male flowers to the eggs of female flowers. One way floral “sex” is accomplished is by the peripatetic flights and landings of birds, bees, and bats, which carry the pollen from flower to flower when they feed on the blossoms’ nectar.

  However, the pollen of many flowers teems with microscopic fungi, viruses, and worms … all seeking to be transmitted into new hosts. When animal pollinators ascend from a bloom—legs and bellies sticky with what is essentially flower semen—these minute pathogens are often along for the ride. When the bee or hummingbird visits the next flower, it deposits pollen … along with a load of these flower STDs.

  What’s really interesting is that these diseases can make plants, for lack of a better word, promiscuous. The white campion flower, for example, is susceptible to a fungus aptly named “anther smut.” A Duke University botanical disease ecologist, Peter Thrall, found that plants infected with anther smut tended to produce larger floral displays. Uninfected plants had punier bunches of flowers. With their big, ostentatious blooms, the flower hussies received (and could accommodate) more visits from more pollinating suitors. By forcing the plant to produce bigger, showier flowers, the fungus was biologically changing its host in a way that made it more attractive to pollinating creatures. This directly benefited the fungus.

  A similar “strategy” may be used by the trypanosome that causes an equine disease called dourine. Infected horses, mules, and zebras suffer fever, genital swelling, lack of coordination, paralysis, and even death. Although it’s now extremely rare in North America and Europe, dourine once ravaged the cavalries of the Austro-Hungarian Empire and swept across the horse populations of southern Russia and northern Africa. In Canada in the early twentieth century, dourine decimated Indian pony herds.

  Dourine spreads when animals mate. Intriguingly, scientists and veterinarians report anecdotally that when dourine is present in a group, the libido of stallions seems to increase.

  How this works may be very similar to how anther smut influences the “behavior” of flowers. Full-blown dourine wreaks physical havoc on the animal … but the early signs of infection are more subtle. A mare may seem perfectly healthy except for a minor vaginal discharge that reveals itself as a wetness around her tail. Mares infected with dourine often keep their tails slightly raised, presumably to ease discomfort from the increased wetness.

  A mare’s raised tail is also a signal of sexual receptivity. So is something else, familiar to every horse breeder, that’s visible when the tail is up. It’s called vulval “winking.” Caused by the vulva’s contracting and releasing, vulval winking happens when a mare is in heat.

  But an under-the-weather, dourine-infected mare, her tail raised and her vulva wet with discharge and perhaps winking with discomfort, may incite randiness in a stallion with her STD-induced f
alse advertising. While the stallion may suffer from the mistake, the pathogen will benefit.

  Sometimes the connection between infection and behavior can seem very roundabout. One of the most perplexing endpoints of many STDs is the destruction of their host’s fertility. You would think this would be a terrible ploy, for two reasons. If a population can’t produce offspring, that usually means the end of the line for the bug. Without a new supply of hosts, where are a bug’s descendants to live? And then there’s the other problem: If an animal can’t have offspring, what would drive it to have sex?

  But bugs’ success is tied to how much their host mates, not to how much their host reproduces. (The increasing incidence of STDs in people over fifty illustrates how these infections need sexually active hosts … not necessarily fertile ones.) A female animal who is having trouble procreating may in fact try harder—that is, have more sex—than one who is already pregnant. If a pathogen can disrupt the pregnancy cycle by inducing miscarriages or preventing conception, it is likely to enjoy the benefits of increased mating attempts. Is it possible that by hindering reproduction certain STDs are actually driving their hosts to have more sex?

  In fact, some veterinary literature supports just that. An STD of deer and other ungulates, for example, puts the females permanently in heat and thus more receptive to sexual overtures. When Brucella abortus causes a cow to miscarry her calf, it makes her ready for a new breeding cycle—sooner than if she had carried the calf to term. This revelation suggests that subclinical infections (those percolating below the surface but not actively causing symptoms)—or even as-yet-unidentified pathogens—may play a greater role in unexplained human infertility and repeated miscarriage than we currently suspect.

  In other words, even low levels of infection might alter sexual function and behavior. STDs are especially good at going deep undercover once they’re inside a body, quietly colonizing it with few overt symptoms. Whether the infections are small and contained or widespread and subclinical, these organisms do affect our bodies and minds in ways that might be unseen to us.

  As a medical student at U.C. San Francisco during the height of the AIDS epidemic there, I was instructed to aggressively dispense safe-sex advice. Even if a patient came in with an earache, I brought sex into the conversation. I recommended wearing condoms and avoiding multiple partners. (Remember that quintessential 1984 line “When you sleep with someone, you are sleeping with everyone they’ve ever slept with”?) I counseled patients to question potential mates (“Do you ever have sex with men?” “Do you use IV drugs?”). A veterinarian can’t warn her patient to wear condoms and interview a sex partner before even getting to first base. But one more preventive technique I used to recommend does have an animal correlate. I was trained to advise that potential partners inspect one another’s genitals for sores and lesions before engaging in sex.

  An animal version of this has been reported in birds. It’s called cloacal pecking† and has been described as a male bird pecking inquisitively at the vaginal opening of a female before mounting her. Some researchers speculate that the fluffy white feathers or prominent “lips” around the cloacal openings of many bird species serve as additional aids for assessing health in a potential partner, since ectoparasites and lesions might show up against the pale background. If soiled by diarrhea or other bodily fluids, these structures would also warn a potential suitor of an unhealthy bird.‡

  Lab studies also show that postsex cleansing might offer a modest level of protection. Rats that are prevented from genital grooming after coitus have higher STD rates than their cleaner counterparts. Many birds preen vigorously after copulation, which some researchers suggest may help do away with bugs trying to hitch a ride on the act. In humans, genital scrubbing does not protect against viral STDs, but it may be slightly effective against bacterial infections. A study of Cape ground squirrels in South Africa showed that the ones having the most sex were also the most frequent masturbators; the researcher speculated that it’s a way to flush out the urethra after intercourse in order to protect the animal from sexual infection.

  A recent study showed that simply looking at a photograph of a sick person caused some people’s immune systems to surge. Indeed, animals may have other ways of visually sizing up the health of a mate. For example, in males, red pigmentation—whether in a grouse’s comb, a house finch’s feathers, or a guppy’s skin—may indicate underlying fitness. These animals’ bodies cannot create the color red on their own. To impart the bright tint, they have to be healthy enough to source and eat lots of red-pigmented carotenoids, found in fruit or shellfish. Conveniently for any females who might be speed-dating with these males, parasites can interfere with the absorption of these pigments. Animals with paler features are in effect advertising their inferior health status.

  But if the thought of colonies of invisible organisms invading your body and controlling your behavior has you reaching for the doxycycline, think again. Our best response to the microbial arms race is not necessarily a scorched-earth campaign.

  In the 1980s, a British scientist shook up the world of microbiology by asking an outrageous question: Can we be too clean? David Strachan was pondering whether hay fever might be related to hygiene and household size. A few years later, a German scientist, Erika von Mutius, was investigating childhood asthma. She was vexed by data that consistently showed that it was most prevalent not in lower-income, more polluted East Germany but, rather, in wealthier, cleaner-living West Germany. The so-called hygiene hypothesis started to circulate, postulating that there are serious consequences to wiping out too many of the microorganisms that have colonized us and our planet for so long. Overusing pesticides, antibacterial agents, and antibiotics, it suggests, kill “good” pathogens along with harmful ones. Plain old better housekeeping and even overly thorough food inspections, the theory goes, create microorganic dead zones. These sterile environments deprive our immune systems, honed over hundreds of millions of years, of necessary daily battles against invaders. And when deprived of external organisms to fight, they sometimes launch an internal attack. An idle immune system will sometimes start attacking itself.

  The hygiene hypothesis, while still a matter of debate, is now being used to explain more than just asthma, allergies, and other respiratory diseases. Upsurges in gastrointestinal disorders, cardiovascular disease, autoimmune disorders, and even some cancers are being traced to it, too. However, no one has really looked at the genital environment—and whether it, too, can suffer from being “too clean.”

  This leads to an intriguing thought. Are some of the pathogens associated with sexual activity beneficial? Most animals have multiple sexual partners—which means that sperm from many different males must duke it out inside vaginas, uteruses, and fallopian tubes to win the conception derby. Conception is not some genteel, quiet pastime; it’s a fierce and unforgiving team sport. The swimmers that win sometimes have assists from microscopic wingmen—the sperm-enhancing microorganisms that live in semen and may be transferred from penis to vagina to penis to vagina. The sexual act may propel the package of semen, but it is then up to the ejected sperm and its microbiological posse to obstruct and destroy competing sperm. Some of these pathogens aid their sperm’s motility, while others act as blockers and killers of competing males’ spermatozoa. And if that isn’t enough, these teams must also successfully negotiate the vagina’s own mix of receptive and defensive microflora.

  This means the microorganisms inhabiting an animal’s urethra or vagina might make the difference between conceiving and not. Or, when there are multiple male partners, determine which of these males’ sperm wins the ultimate prize: fertilization, the chance for his DNA to advance to the next round.§

  This made me wonder whether striving for an aseptic genital environment could, in fact, be harmful (beyond the well-known risk of a yeast infection after antibiotic therapy). The human immune system fully matures between the ages of eleven and twenty-five—just when sexual activity is movi
ng into full gear, bringing with it a barrage of new, unfamiliar microorganisms. The hygiene hypothesis demonstrates the risks of underexposure to pathogens of the respiratory and GI systems. Might there be a genital version of the hygiene hypothesis? Could a “just right” mix of microorganisms in your genitals improve your chances for conception or help select the highest-quality sperm for your soon-to-be-conceived child? Might there be a place for a probiotic product to aid conception—similar to the products that improve digestion in the gut microbiome? Or maybe there’s an intriguing flip side: Could studying sperm-killing micropathogens in animals lead to new contraceptives?

  It’s important to stress that, given the threats STDs pose to human health, this is not an argument for unsafe sex. Condoms save lives. Physicians and educators must resoundingly continue to emphasize the absolute necessity of safe-sex practices. But physicians should join veterinarians in considering the long-term ecological perspective of therapies and remain open-minded about unlikely or unexpected consequences of intervention.

  As Janis Antonovics, a disease biologist at the University of Virginia, told me, “There is no imperative to cure disease in natural populations. Disease is natural!” Doctors first and foremost have a responsibility to treat individual patients. But ecologists like Antonovics take the pathogen’s-eye view of infection. As he explained it to me, every time we perturb a system, by extermination or prevention, there is always a repercussion. An individual may see an immediate benefit from a round of antibiotics, but invariably, necessarily, killing off those organisms causes some unintended side effect, either immediately or down the line. Sometimes it comes back in a more virulent form. Infection (and all the viruses and worms and bacteria and other organisms that create it) is a complex, interconnected, multidimensional web. Tugging out one strand alters the architecture of the entire network.