For arthropods, male-versus-female sex has more to do with infections than it does with genes or chromosomes.
For arthropods, male-versus-female sex has more to do with infections than it does with genes or chromosomes.
This blog post is excerpted from Gerald N. Callahan's Lousy Sex: Creating Self in an Infectious World.
This morning, I am escorting a wood louse out of my kitchen and onto the lawn. It is early spring. The air is warm and full of promise, and as I launch the balled-up creature lawnward, my thoughts turn to sex. Unusual sex, mysterious sex, infectious sex.
Humans will use almost any excuse to think about sex. But wood lice will never be voted among the top ten reasons for this. Wood lice—roly-poly bugs, pill bugs, potato bugs, sow bugs—are those armor-plated crustaceans that scatter, on fourteen jointed legs, like cockroaches when the light hits them or, when we poke at them, curl themselves into impenetrable scale-covered balls.
Sort of creepy. But it gets even creepier. Wood lice harbor one of the deepest and darkest tales ever told about animal sex. Irresistible, uncontrollable, unforgettable tales of sexual exploitation.
Sex, it turns out, isn’t always about who you are or where you’ve come from. Among wood lice, sex has a lot more to do with where you’re headed for and what you’ve got—or, more accurately, what’s got you.
Nearly 3,500 different species of wood lice carpet our planet with their scaly hides. And—crawling through our gardens or the moist soil lining our homes’ foundations and breathing through gills—wood lice are hiding something, something sexy.
If you spend time among the detritus that has collected in the dark and damp spots around your yard, you’re bound to encounter wood lice—they’re everywhere you’d just as soon not be. And if you spend a lot of time poking through the leaf mush and garden goop, you might notice that besides their slightly prehistoric appearance, there is something truly weird about wood louse sex.
Surprisingly, it’s pretty easy to find out if a wood louse is a girl or a boy. According to Invertebrate Anatomy Online here’s all you need:
When you nudge the living isopod (wood louse), the creature will reflexively curl up into a ball. A short while after you drop the bug into the culture dish, it will uncurl, almost always on its back. This is where things get exciting. If you want the louse to hold still, you’ll have to resort to the chloroform-soaked cotton. Personally, I like them squirming. Now just slip the culture dish under the microscope and take a close look at the critter’s pleon—the last seven plates at the rear on the underside.
The long slender endopods of the first two pleopods of males are modified to serve as copulatory organs, or gonopods. The same is not true of females.
It's just that simple.
I am not certain what the applicator stick is for. Maybe it just makes the whole thing seem a little less prurient, a little more clinical.
After you have done this a dozen or so times, it gets really easy. Also, after you have done this a dozen or so times, you will begin to notice something odd. Every louse you picked up has turned out to be a female louse. Beginners may doubt their technique at this point. They shouldn’t.
Most species of wood lice are all or nearly all females. The few species of wood lice that do produce males produce very few compared to females. For many humans, this discovery is disconcerting. We take for granted that the nature of evolutionary forces, reproductive advantage, and old-fashioned sexual predilections will always lead to male:female ratios of about 1:1. Wood lice take nearly nothing for granted, and among wood lice, sex ratios never naturally approximate equality. We also take it for granted that whether a child of ours becomes a boy or a girl is a result of something we as parents did (that whole chromosome thing). But among wood lice, sex is completely out of their control.
As it turns out, sex is also beyond the control of most insects; many spiders, mites, and ticks; a fair number of parasitic worms; a few shrimp; and some lobsters. For all of these animals, sex has nothing to do with any of the things we think of as essential to sex.
Wood lice, if they could, would love to go along with the rest of us, spread their chromosomes far and wide and lay down equal numbers of boy and girl eggs. But this world rarely gives wood lice such an opportunity. If allowed, wood lice—like birds—produce males that have two Z chromosomes and females with one Z and one W chromosome. And left to their own devices, wood lice produce about equal numbers of lousettes with ZZ and ZW chromosomes—nearly equal numbers of males and females.
Trouble is, wood lice aren’t allowed.
Instead of a chromosomal grip on the tiller of their own sexes, the world has given wood lice an infection. A very small thing, something that people overlooked for years, usually takes control of wood lice sex before chromosomes even get a shot at it. So the lack of “long slender endopods” that you observe under your microscope was no mistake. Male wood lice are a rare commodity.
Until the 1970s, this skewing of wood lice sex ratios remained completely mysterious. About then, a microbiologist gone rogue decided to take a close look at wood lice eggs. What he found there forever changed the way we think about sex, if not lice.
Inside wood louse eggs, this microbiologist found fistfuls of bacteria. Not a common thing with eggs. And one particular type of bacterium predominated—a bacterium called Wolbachia. In spite of the fact that no one had ever seen anything like this with insect eggs, these bacteria didn’t stir up much interest among microbiologists or entomologists. A few years later, though, another miscreant microbiologist looked to see what would happen if he treated wood lice with antibiotics to kill the bacteria.
Amazingly, wood lice treated with antibiotics began producing about equal numbers of ZZ males and ZW females. Whatever was wiping out wood louse males, antibiotics cured it. Among wood lice, sex was a disease. Even worse, an infectious disease.
This didn’t fit with anybody’s model of all-female societies or, for that matter, with anyone’s idea of rollickingly good sex.
To deal with their disappointment, and to cover the evidence that males might not matter so very much, microbiologists explained all of this as a rare example of a bacterium somehow skewing the sex ratios of one species of wood lice—one of those “gee whiz” sorts of things, but of no real importance to understanding entomology, let alone sexual reproduction. After all, wood lice are, well, lice. How important could any of this be?
That explanation didn’t hold up long. When scientists started looking elsewhere for Wolbachia, it turned out that most species of wood lice, most species of insects, many shrimp, some lobsters, some spiders, and a lot of little mites all have an infection, an infection that makes most of them into little girl lice or shrimp or spiders or mites.
The Low Road to Domination
The more places microbiologists looked for Wolbachia, the more they found it. And when the investigative dust settled, it was apparent that Wolbachia is the most common infectious bacterium on Earth. And far and away the world’s champion sexist.
Hardly an evolutionary blip. Rather, the interaction between Wolbachia and its host is one of the most, if not the most, frequent symbiotic relationship(s) in all of biology. Like people and cell phones, almost every bug has a constant companion.
Wolbachia infects about 65 percent of all insects. Insects are by far the most numerous of all multicellular animals—about 1,015 individuals and as many as 30 million different species. That means that about 6.5 × 1,014 animals (equivalent to 100,000 times the number of human beings on Earth) and at least 1 million species of animals are all infected with Wolbachia—each and every one making its living only at the whims of a bacterium. And then there are the infected spiders, the mites, the ticks, a fair number of parasitic worms, more than a few shrimp, and several lobsters, all equally infected and equally prone to the tricks of bacteria.
That means that Wolbachia infects most of the animals on this planet. Which in turn means that, among us animals, most of us have absolutely no say in whether we end up in the pink or the blue crib. Bacteria determine sex for most of us. So while we call this an abnormality, an infection, and a disease, in truth it is simply the way of life for most of us. Regardless of what Sister Irene may have told us in high school, it’s microbes, not chromosomes, that hand out sexes to animals.
Just when the first bacterium took over the reins of a wood louse’s sex life can’t even be surmised. But how so many animals continue to be infected is not so inaccessible. Wolbachia live, among other places, inside the eggs of all of its hosts. So every time a baby louse, mite, wasp, lobster, and so on is born, it is already infected with Wolbachia. That explains how this bacterium continues to infect so many animals. But why do most of these animals end up as females? Wolbachia, it turns out, is an obligate intracellular parasite—it can only make a living inside of someone else’s cell. Wolbachia doesn’t have everything it needs to make more Wolbachia. What it lacks, someone else must provide. So to keep their families going, each of these bacteria have to find a room (cell) of their own inside of which they will make baby Wolbachia.
Outside of cells, Wolbachia die. That presents another problem. How to get from louse to louse? For Wolbachia to move from one animal to another, it must move inside of a cell. Lobsters and shrimp and wood lice don’t transfer cells from one to another, except during mating.
That’s where Wolbachia saw its opportunity. If it could find its way into sperm or egg, the bacterium was on the high road to a new generation and a bright future. Here was an obvious solution.
But only eggs have enough cytoplasm (the semi-liquid stuff that surrounds the nucleus) to accommodate Wolbachia. Sperm are just little outboard motors attached to DNA. Because of that, sperm have no room for bacteria. So the future of Wolbachia lay with the egg.
Solving the egg problem, though, wasn’t good enough. If sperm and egg came together and made a male wood louse, it was a dead end for Wolbachia. That’s because any bacteria inside of those cells would be squeezed out as the new male’s spermatogonia got small enough to become sperm. That meant that at least half the time, Wolbachia’s journey would end in the black pit of the belly of a sperm. Evolutionarily, if not personally, that was a problem.
To Wolbachia, the solution seemed obvious—limit the number of males. And the bacterium immediately set about developing an array of ways to do that. One of the first tricks Wolbachia put to use was a process called cytoplasmic incompatibility.
Without Wolbachia, most matings between male and female wood lice are productive. But among infected species, when a Wolbachia-infected female mates with an uninfected male, nothing happens. No boy wood lice, no girl wood lice, nobody—cytoplasmic incompatibility. Wolbachia do that. Only when an infected female mates with an infected male—providing the same species of Wolbachia infects both sexes—does a multitude of new tiny sow bugs come into this world. Somehow, Wolbachia see to it that if one parent is uninfected, Dad’s chromosomes disappear as the embryo is just getting started. And that means that new lice appear only when the conditions are just right, just right to produce one more litter of blue-bonneted lousettes.
And that’s good. But not good enough.
The Power of Parthenogenesis; or, "L" Is for Louse
To improve its own odds of survival, in some species of wood lice and wasps, Wolbachia has simply blown the males clear out of the picture. In these wasps and wood lice, Wolbachia turns all developing babies into ZW baby girls. On top of that, in these critters, Wolbachia infection confers the power of parthenogenesis on each new female. That means that in these species every female can produce more baby lice or baby wasps without the need for a male partner. Parthenogenesis is females making more females, making more females, and so on. Babies, lots of them, and no need for sex.
In these wood lice and wasps, not only has an infection changed the sex of the young, it has also driven these animals from the ranks of the sexual reproducers and has returned them to their past as asexual beings producing only female young. No need for any males.
Treatment with antibiotics will force some female wasps and wood lice to revert to sexual reproduction and hatch male and female animals that have to find one another to make more like themselves. But in other wasps, Wolbachia has found a way to close all avenues to the past, even those that might have been reached through antibiotics.
Asobara tabida Nees is a relatively common wasp that lays its eggs in fruitfly larvae—little worms that hatch from fly eggs. As the young wasps develop, they slowly consume the living fly larvae and emerge as fledgling wasps, already infected with three species of Wolbachia. Though antibiotics cure the sexes of some other infected species of insects, treatment of A. tabida with antibiotics makes the females sterile. In fact, elimination of Wolbachia causes these wasps to stop making eggs completely. It seems that on top of everything else, Wolbachia has also taken control of oogenesis (egg making) in this species. So if the bacterium cannot have its females and its future, then neither will the wasps have theirs.
From a simple bacterial infection, this relationship has evolved to a fully dependent symbiosis between wasp and bacterium. Together, these individuals have reached a point where neither can live without the other. And of course, that relationship is absolutely dependent on the wasps’ continued production of females, which they happily provide. Infectious sex, infectious egg laying. What was once two has become one.
Wolbachia has also established essential long-term relationships with several filarial nematode worms, including Brugia malayi and Wuchereria bancrofti (the worms that cause elephantiasis), and Onchocerca volvulus and ochengi (the worms that cause river blindness in places like Guatemala).
Elephantiasis (aka lymphatic filariasis) is a terrible parasitic disease with enormous swelling of one or more limbs as a result of infection and blockage of a person’s lymphatic vessels. River blindness (onchocerciasis) is the second leading infectious cause of blindness in the world (trachoma is number one). River blindness also results from infection with a filarial worm. Damage to the eyes is only one of many, many problems caused by O. volvulus. Surprisingly, antibiotics kill the worms that cause both of these diseases.
But it isn’t because the antibiotics kill the worms themselves. As is the case with all other worms, antibiotic compounds have no direct effect on these worms’ physiology. But the worms have developed a complete dependence on an infection with Wolbachia for their survival. On top of that, O. volvulus obtained from the blood of infected people treated with doxycycline (a powerful antibiotic) could no longer cause river blindness. It appears that the human interaction with the Wolbachia inside the O. volvulus worms is an essential piece in the puzzle of river blindness. No bacteria, no river blindness.
Infectious femininity, infectious blindness, macabre symbiosis.
Two-spotted lady beetles are sometimes mistaken for ladybugs, an easy mistake to make with these red- and black-spotted insects. That misidentification leads people, for no apparent reason, to treat these beetles much better than people treat most beetles. Perhaps we would be less likely to treat these beetles so kindly if we realized that two-spotted lady bugs, even as they crawl across our palms, are systematically killing all of their male eggs—a seemingly heinous act.
In truth, though, the beetles can’t help themselves.
Most two-spotted lady beetles, along with Acraea encedon—beautiful orange and black butterflies—produce only female offspring with normal female sex chromosomes. Antibiotic treatment causes both species to begin to produce genetically normal male and female beetles and butterflies in nearly equal numbers. That suggests that most of the time something bad is happening to about half of the eggs belonging to these butterflies and beetles. In other words, it seems very likely that all of these female insects are producing equal numbers of male and female embryos, but the male embryos just don’t make it through to hatch as live animals.
Inside these bugs and beetles, the ever-resourceful Wolbachia has found yet another way to limit the number of males. In some beetles and butterflies, Wolbachia simply kills all the male eggs. And it turns out that two-spotted lady beetles and A. encedon butterflies are just two examples. Wolbachia drives many other insects to murder their male eggs.
By the way, among male-killing species of bugs—as they hatch, the females dine on the dead eggs of their would-be brothers. So among the male killers, nothing goes to waste, except for the occasional male ego.
And still that wasn’t enough for Wolbachia. More ways of eliminating males had to be found if the bacterium was to achieve its full potential.
In some species of insects, Wolbachia simply changes genetic males into females. As I said before, without infection most insects produce ZZ males and ZW females in nearly equal numbers. But if you examine some Wolbachia-infected insects, you find that—even though the bugs continue to produce equal numbers of ZZ and ZW animals—all of the offspring are females.
Even when faced with the daunting task of overcoming genetic predispositions, Wolbachia is unfazed. It seems that Wolbachia has found some way to manipulate hormonal control during male development. As a result, even though the baby bug has male genes, Wolbachia overcomes that predilection by several different and generally poorly understood mechanisms.
One trick some species of Wolbachia use is to close the spigot on male androgens and force the developing bugs on the female railroad. If these were human beings, we’d call them pseudohermaphrodites and label them as biological abnormalities. Among these insects, pseudohermaphroditism is the norm. And if antibiotics or some other killer destroys the infecting Wolbachia during fetal development, the baby bugs are all intersex.
Male, female, or in between: all under the control of a bacterium. All of it the result of an old but persistent infection. In the end, though, the result is a whole population where chromosomal differences don’t correlate with anyone’s sex. It doesn’t matter whether an animal is ZZ or ZW. They are all females, and all infected with Wolbachia. In spite of our fondness for stories of chromosomal supremacy, our insects suggest that genes, by themselves, don’t mean squat.
If that weren’t enough to subvert your ideas about sex, it turns out that Wolbachia isn’t the only bacterium that can change an animal’s sex, not even close. The false spider mite Brevipalpus phoenicis is a tribute to the force of life, the force of life and the power of compaction, that is. These mighty mites are tiny—about 3/250 of an inch long by 16/2,500 of an inch wide, which is about as wide as a human hair and about one-third the size of the largest bacterium ever discovered.
False spider mites infest mostly plants where they can do a lot of damage, especially to citrus plants. I assume they are called false spider mites because they do look a little like spiders, but they aren’t, they’re mites, another sort of arachnid.
When entomologists first studied the false spider mite, the researchers were amazed to find that all of these animals were haploid females. Most animal cells are diploid—meaning they have an even number of chromosomes, half of which came to them from each parent. Normally only sperm and egg are haploid and capable of performing their functions with only half the normal number of chromosomes.
False spider mites were the first animals ever found to be uniformly haploid—meaning that each cell inside of each mite has only one copy of each chromosome and only one copy of each gene. That shook the foundations of a couple of aspects of evolutionary biology.
Of course, maintaining a strict haploid existence precludes even the occasional sexual tryst. So, a long time back, false spider mites took up the practice of parthenogenesis, producing children without sex—all of them females. Among these mites, apparently alone among all the animals, there are no chromosomal differences between gametes and somites—no differences between the reproductive cells and all the rest of the cells of the body.
That drove the evolutionary biologists to probe further. How could this have possibly happened? How could an entire species of what must have once been diploid animals be reduced to these hapless, haploid remnants? Actually three remnants, since there are three closely related groups of false spider mites that are all haploid.
False spider mites’ eggs seemed like a good place to start trying to answer those questions. What those biologists found inside false spider mite eggs opened another door everyone imagined shut for millennia. False spider mites’ eggs were full of bacteria. Not Wolbachia, surprisingly, not even a distant relative of Wolbachia, but a whole different phylum of bacterium—Cytophaga-Flavobacterium-Bacteroides. Full of bacteria.
Thousands of these bacteria filled the cytoplasm of every false spider mite egg the scientists examined. Out of curiosity, the scientists treated some of these eggs with antibiotics. For comparison, they also hatched out some eggs that had seen no antibiotics. Infected eggs all developed into females, while “cured” eggs all developed into males.
Even though every false spider mite today has only one copy of each chromosome and only one copy of each gene, these experiments gave clear evidence that once upon a time, these mites had been sexual reproducers. Once male and female false spider mites had walked proudly across the fields and the fruits of this Earth. But no longer. A strain of Bacteroides (another bacterium) changed all of that. Who knows how long ago the last natural male false spider mite fell prey to an infection, an infection that slowly, or maybe not so slowly, changed the course of false spider mite history forever. Gone was sexual reproduction, gone were homologous pairs of chromosomes, gone was romance as we know it, gone were male false spider mites—all gone, gone forever because of an infection. And today, without that infection, all of the false spider mites would disappear within a single generation.
The Problem with the Past
In the classroom, most of us learned three things about sex as we made our way through our science courses. First, since everybody—or at least everybody who is anybody to us humans—uses sex to reproduce—there must be some enormous evolutionary advantage to this sexual reproduction thing. Second, males and females always arise in about equal numbers so everybody gets an equal shot at reproducing. The same must be true for everyone else. And last, the thing with its hand most firmly on the throttle of gender control is a chromosome.
The textbooks and the teachers we learned from, though they meant well, were wrong.
The vast majority of animals in this world have dramatically skewed sex ratios, numbers nowhere near the supposed ideal of 1:1. The majority of the animals in this world are females—females who have given up on sex, but whose species still flourish. For most of us, chromosomes have nothing to do with sex. Instead, it’s all about bacteria, mindless bacteria bent on their own success.
Sex for most of us is, in fact, an emerging infectious disease. Eggs full of bacteria, bacteria whose sole interest is making more bacteria. To them we are nothing more than a vehicle, a vehicle designed to carry them from place to place and to move them from egg to egg. We persist only because we can deliver these bacteria into our children and the world beyond. Our past may have been filled with sterile misunderstandings about sex, but our future is septic.
. . .
In nearly slow motion, the wood louse rolls through the air toward the newly green lawn. Now, I am reminded of Strauss’s Blue Danube and Stanley Kubrick’s epic film 2001: A Space Odyssey. The scene where the shuttle from Earth and the space station lock into in a slow minuet.
The wood louse hits the lawn, bounces upward once, and falls back. For a few seconds, it just lies there—feigning death. Then slowly, the isopod uncurls it chitinous body and rights itself.
Something like David Bowman’s last words rolls through my brain. In Arthur C. Clark’s book version of 2001, Bowman—the sole surviving crew member on the deep-space probe Discovery One—at last arrives near Jupiter and finds a monolithic stone left in orbit there by some other intelligence. David dons his space suit and, inside one of the extravehicular activity pods, jettisons himself from the giant ship Discovery.
The music inside my head switches to that of another Strauss—Richard—and Also Sprach Zarathustra.
As he nears the monolith, David’s ragged breaths rasp like bellows through the telecommunications device inside his space suit. Finally, directly above the anomaly near Jupiter, from the oval window of his EVA pod, he stares into the monolith.
“The thing’s hollow,” David says. “It goes on forever—and—oh my God! It’s full of bacteria!”
Gerald N. Callahan is a professor in the Department of Microbiology, Immunology, and Pathology and the Department of English at Colorado State University in Fort Collins, where he lives with his wife and dog. He is the author of Lousy Sex: Creating Self in an Infectious World; Between XX and XY: Intersexuality and the Myth of Two Sexes; Faith, Madness, and Spontaneous Human Combustion: What Immunology Can Teach Us about Self-Perception; Infection: The Uninvited Universe; and River Odyssey: A Story of the Colorado Plateau and co-author of Basic Veterinary Immunology.