Sex on Six Legs

by Marlene Zuk

  In addition to studying the ants as a scientist, Herbers has questioned the wisdom and accuracy of the name slave-maker ants. She is not alone in this regard; Hölldobler and Wilson point out, "It is traditional to use the expression slavery for the exploitation of one species by another. In the human sense this is not slavery but more akin to the forcible domestication of dogs and cattle by humans." They go on to detail situations in which ants use the labor of others from the same species, but the term slavery is clearly limited in its applicability. Some entomologists use the more technical jargon term dulosis to refer to the process, whether within or across species, but most scientific journals still call it slave making.

  Herbers is not just concerned about the use of the word slavery by scientists. She questions its suitability given its obvious connotations of human activity. At public lectures, she often is asked about the parallel between ant and human slavery, a parallel she always decries. She has come to the conclusion that we would all be better off abandoning the metaphor and terminology entirely, because of its emotionally loaded overtones. As an alternative, Herbers proposes the term pirate ant, since human pirates also make raids and steal cargo, often killing some of the victim ship's crew. Scientists could continue to discuss raiding parties, captives, and booty, without recourse to the loaded terms that certainly bring the public up short. I am in agreement with the distaste for the word slavery in nonhumans, and use it here only when the original authors use the term, so as not to rewrite their usage.

  Regardless of its social baggage, however, another problem with calling the ants slave makers is that, as with the army ants, it gives an entirely incorrect view of what the ants themselves are doing. Hölldobler and Wilson's point about domesticated animals versus forced labor from members of the same species aside, most biologists, including them, classify the behavior as a kind of parasitism. In other words, the so-called slave makers are acting like exceptionally free-roaming tapeworms. Like the tapeworm, the slave makers, at least the obligate species, make their living entirely off of another organism, the host. But instead of traveling passively from one host's intestinal tract to another via, say, a contaminated bite of meat, the ants take matters into their own six legs. The slave raids, with the excited workers rushing to and fro with their cargo of pale cocoons, are just a more visible and dramatic version of the worm in the gut ensuring it will have someone to provide it with a steady supply of meals for the foreseeable future. Even Crompton notes that "a slave-raiding expedition is not really a battle, it is a routine commercial undertaking."

  Admittedly, this analogy is not perfect, and the ants are what scientists call social parasites, rather than internal ones. Cuckoos and cowbirds are the most familiar examples of such animals: the cuckoo female lays her eggs in the nest of another bird species, exploiting the parental behavior of the host, who rears a genetically unrelated chick. The hosts have, in a sense, adopted the enemy to their own advantage, gaining the labor of others at little expense. And Maeterlinck points out that the captive ants do exactly the same thing that they would be doing in their own nest, namely, feeding the workers and caring for the queen. Their lives are no harsher than they would be in their own nest, and the everyday life of any ant is pretty grim by anthropomorphic human standards at least. But those pejorative declarations about degeneracy from Crompton and Maeterlinck fit right in with this point of view. Tapeworms and many other parasitic organisms have reduced limbs, eyes, and other organs, a state of affairs that probably evolved because the appendages are unnecessary, maybe even an impediment, in the dark cozy confines of the host's gut. Crompton's prediction about the extinction of the slave makers may be off the mark, since of course parasites show no signs of going out of business. Seeing slave making as a form of parasitism gives rise to the unsettling thought that, by the same token, we are a kind of slave to our own pathogens.

  Viewing the interaction as parasitic not only sidesteps the terminology melodrama, it clears the way for asking other interesting questions. Herbers and her colleagues have examined variation across the range of several species of pirate ants regarding which species they exploit, and, as with a disease-causing organism, talk about the "virulence" of different raiding species. Just as anthrax is more virulent than athlete's foot, by doing more damage to its host, a more virulent social ant parasite kills a larger proportion of the adult ants at the nest it raids.

  With postdoctoral scholar Christine Johnson, Herbers introduced two different slave-making species that parasitize the same host species into outdoor enclosures in a field in Ohio. The enclosures had one or the other slave-making species or both at the same time, along with the host species. The researchers then waited to see how the host species did, predicting that the presence of both slave-maker species would be the biggest burden on the host ants. Much to their surprise, the host colonies did better when both parasite species were present together. Johnson and Herbers speculated that the two types of slave makers might have competed with each other, to the detriment of both, leaving the host ants to prosper unmolested. This kind of complicated interaction among several species is becoming increasingly interesting to scientists, since it suggests that we need to look at more than just one species at a time to understand an animal's ecology. The researchers concluded that variation in the abundance of slave makers could affect "hot and cold spots" of ant abundance in the forests where the ants occur.

  Just such geographic variability in ants was the subject of a study by Susanne Foitzik, now at Regensburg University in Germany but formerly another postdoctoral scholar working in Herbers's laboratory. Foitzik and others have recognized that the ants are a good way to study ways that a host and parasite can influence the evolution of each other, in what's called a coevolutionary arms race. After all, one wouldn't expect the host, or exploited species, to just sit back and take it—for example, we evolved an entire immune system to resist the attacks of viruses and bacteria. Other kinds of hosts of social parasites show varying degrees of defenses against the parasite; some cuckoo and cowbird hosts recognize and reject the interloper's eggs, while others seem to be oblivious to the gigantic size of the parasite chick relative to their own offspring and valiantly stuff food into the cuckoo chick's gaping maw at the expense of their own reproduction.

  Foitzik and her coworkers looked at the ways that the slave, or host, species varied in its ability to defend itself against the slave makers. They were interested in whether the defense mechanisms were the same in different places, regardless of the intensity of the raids by the slave makers, or whether each pair of host and parasite populations evolves a unique way of interacting, with a new arms race in each locale. They compared colonies of a raiding species and its victims in the Huyck Preserve in New York state with those in West Virginia. More and larger colonies of the slave-making species occur in New York, which should make the pressure on the host species more severe, since they are being raided more frequently. The slave-making ants in turn can kill the queens of their hosts without too many repercussions, since many colonies of potential victims are also present.

  The scientists found that the coevolution between host and parasite was in fact different in the different places; in New York, a guard ant was more likely to be found protecting the host nest entrance, and in turn the New York slave-making ants took more of the brood from the nests they raided. The host defenses were also more aggressive to the initial scouts sent out by the raiding parties. "Ironically," write the researchers, "these host ants are probably killed by enslaved conspecifics [members of the same species] that accompany ... workers on raids, rather than by the slave-makers themselves." The defenses, however, weren't unique to a particular set of nests, supporting the idea that universal defense mechanisms evolve throughout the population.

  The idea that the hosts could defend themselves against the raiders wasn't given much credence until recently, and it's tempting to speculate that the lack of exploration of the idea came from people clinging a little too
tightly to that slavery analogy. Slave rebellions are risky and scarce. But it's commonplace to imagine a host and parasite, for example, the worm inside the gut of a mouse, continually evolving ways to attack or defend against each other.

  Whether you think of it as piracy, parasitism, or slavery, capturing live individuals of another species and benefiting from their labor requires a complicated set of behaviors. How did such a practice evolve? Charles Darwin offered the first potential explanation in The Origin of Species, proposing that the ancestral slave makers first took the pupae as prey. When some of the pupae accidentally escaped detection back in the host nest and became adult workers, they were not perceived to be foreigners and, hence, began doing their normal ant activities, which made the colony as a whole prosper.

  Another possible route to the evolution of piracy is via the territorial battles that commonly take place between colonies of the same species. Ants and other social insects usually have very strong loyalties to their own colony and will attack intruders that smell like they come from a foreign nest. If a new colony is established too near an existing colony, fights between the workers of the two groups can result, and several scientists have suggested that this generally pugnacious behavior could have evolved to be directed at ants of other species as well. If the two species were closely related, and hence shared a more recent common ancestor, the likelihood of them also becoming tolerant of a captured pupa or larva is increased, because the captive would smell more familiar.

  Jeannette Beibl, a researcher at Regensburg along with Foitzik, examined the DNA of numerous slave-making species. They and colleagues R. J. Stuart and J. Heinze determined that the practice evolved independently several times in different groups of ants, some relatively recently, at least by evolutionary standards. This variation suggests that different selection pressures might have caused slave making to evolve in the different species.

  Six-Legged Constables

  IF THE army ants aren't a real fighting force and the slave makers are just parasites with an uncanny resemblance to their hosts, do treachery and aggression exist at all for the social insects? The answer is a resounding yes. The carnage is subtle, but far more devastating in its after effects than even the most formidable slave-taking raid. In evolutionary terms, loss of life is not nearly as injurious as loss of reproduction. The social insects, with their suicidal colony defense and sterile workers, have perplexed evolutionary biologists since Darwin. While biologists have mostly explained the benefits of such extreme cooperation for the individual colony members, those busy little virgin bees and ants still turn out to show some enterprising forms of rebellion.

  Although worker ants, bees, and wasps cannot mate, they often possess functional ovaries and can produce their own eggs. These unfertilized eggs develop into males, because throughout this group of insects and a few others, daughters have two copies of each chromosome, like humans and other vertebrates, and develop from fertilized eggs, but sons have only the mother's genes and, in effect, have no father. (I often give my animal behavior students an exam question that asks whether it is true that a honeybee male has a grandfather but no father. The ones who get it are triumphant, often hammering the point home in far more text than necessary, while the ones who don't flounder in ever-widening circles of confusion; one ended up declaring in apparent despair, "No, every animal has a father, if they didn't have a father they wouldn't have a mother and then what would happen?")

  This genetic oddity means that workers are often more closely related to each other than they are to their own offspring, although the exact proportion of shared genes varies depending on how many males have mated with the queen. The real genetic payoff comes, as I pointed out in an earlier chapter, not from the workers helping to rear their sterile sisters, but from production of the future reproductives, the queens and drones that will leave the colony and found a nest of their own.

  Under some circumstances, therefore, it is beneficial to an individual worker to lay some eggs that will become male reproductives. But the other workers would pass on more of their genes by investing in their brothers, the sons of the queen, rather than their nephews, the sons of their sisters. So you might expect that workers would sabotage each others' efforts to slip a few of their own eggs into the hive. Indeed, Francis Ratnieks and Kirk Visscher documented exactly such behavior, termed worker policing, in honeybees. The bees are able to tell which eggs are laid by the queen and which by their sister workers and will remove the latter and prevent them from developing. Visscher and Reuven Dukas discovered that the workers can even detect the degree of ovarian development in their sisters and act more aggressively to the ones that are on the verge of producing their own eggs.

  Ratnieks, along with Tom Wenseleers, took the idea of worker policing further. They pointed out that the better the workers are at stopping each other's attempts at reproduction, the more likely it is for workers to give up, in effect, and simply put all their efforts into the queen's offspring rather than try to produce their own. To test this idea, the scientists compared the proportion of egg-laying workers in ten species of wasps and the honeybee; the insects vary in the effectiveness of worker policing in the nest. As they predicted, workers from species in which the policing is stringent are much less likely to try to lay their own eggs in the first place. The scientists conclude that the insects "provide evidence for something that has proved notoriously hard to demonstrate in human society: that better law enforcement can lead to fewer individuals behaving antisocially."

  Ratnieks and Wenseleers also noted that the workers can control each others' reproduction in a different way, by regulating which female eggs end up as queens and which as workers. In many, though not all, social insects, this caste difference is determined during development, with future honeybee queens, for example, placed in larger cells than the plebian workers and fed more of a special substance called royal jelly that jump-starts their growth. Reproducing oneself, rather than caring for the young of others, is an attractive evolutionary prospect, but developing into a queen is only part of the process. It's rather like becoming a movie star: being stunningly beautiful, while essential, is no guarantee of red carpet status. Only a tiny fraction of the queens produced will actually make it to the Oscar-winning equivalent of starting their own hive. But it's not good for the colony if too many individuals become queens, because queens don't do any of the foraging, cleaning, or other mundane tasks of daily life. And yet, as with eager celebrity wannabes, the starlets rush to audition. As Ratnieks and Wenseleers put it, "The lottery to reproduce is so attractive that many more enter than could possibly win the prize of heading a new colony." Policing by the other workers prevents too many queens from being reared, because the larger cells in the comb for rearing queens are strictly limited.

  A tropical stingless bee called Melipona provides an elegant illustration of the scope and limitation of policing. Unlike honeybees, which are reared in wax cells that are open at the top so that the workers can feed the larvae a bit at a time over their development, the stingless bee queens are about the same size as workers and are reared in sealed cells, each of which contains its own ration of food. The female Melipona thus develops into an adult without interference from other bees and can become either a queen or a worker. As a result, up to 20 percent of females are aspiring queens. But grim reality sets in once they emerge from their virginal chambers: lack of policing beforehand means that many of the new queens are set upon by the workers and torn limb from limb. The policing ameliorates this carnage by preventing too many queens from being produced in the first place.

  Punishment of cheaters who try to reproduce on their own in a social insect colony is not confined to bees. Ordinarily, only queen ants produce a particular chemical on their body's surface to indicate their reproductive status. But if a worker's ovaries develop and she begins to lay eggs, the other workers detect the same odor on her body and attack their sister. Adrian Smith, Bert Hölldobler, and Jurgen Liebig painted worke
rs with the telltale compound and induced the aggression, showing that the odor is indeed the trigger for detection of cheaters. In a colony with its queen removed, however, the newly reproductive workers are left alone.

  Ratnieks and Wenseleers ask, "Can humans learn anything from insect policing? The principal lesson seems to be that policing is a common feature of social life and helps to resolve the conflicts caused by the transition from individuals to societies.... Po-licing in human societies has been used by repressive regimes to sustain inequalities, as demonstrated by the negative connotation of the phrase 'Police State.' But a human society in which policing is used to promote greater equality and justice may not be an unattractive prospect." Of course, the conflict between the good of society and individual freedom is an old one, and not likely to be settled by observations from the beehive. My take on the sinister world of Big Sister is that such behavior is far more deadly than the army ants swarming over every living thing in their path. Who needs nuclear weapons?