The Hive Mind

Feature / by Benjamin Phelan /

Is understanding the selfless behavior of ants, bees, and wasps the key to a new evolutionary synthesis?

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Evolutionary Biology has largely been a historical science, built on inferences of the usually unobservable and protracted competition between genomes. The debate over multilevel selection, group selection, and inclusive fitness hinges not just on the best mathematical description of the most elaborate species we see today, but also on what vexed Darwin so devilishly — the origin of eusociality.

“That’s the crux of the question,” says Jim Hunt, a wasp researcher at North Carolina Statue University. “The anathema that is held by kin selectionists for group selection denies a role to multilevel selection in the appearance and elaboration of sociality. That doesn’t cut it.” He’s confident, he says, that multilevel selection had a role in the evolution of today’s superorganismic ants. But studying them is fraught, he says, “because they are well beyond the eusociality threshold, and so they don’t reflect what might have been the ancestral condition. Ants being smaller and having poorly developed ovaries, or no ovaries at all — these are traits that have been selected for in history.” Hunt calls ants and honeybees “okay” for studying the preservation of eusociality, but not for studying the origin. For that, he says, one must look at wasps.

Certain paper wasps, which are eusocial but without the elaborate caste systems and enormous colonies typical of ants, offer unique insights into how Hymenoptera became eusocial. Studying them enables Hunt and his colleagues to table the grander issue of divining what overarching theory governs evolution in favor of directly observing some of the processes that constitute it. Genomic competition over time produces novel traits, but it is not the only force that does so. Genes are turning on and off all the time in living organisms, and some think the pattern of their expression is just as important as the historical process of selection among competing genomes.

“Hamilton’s rule, that famous thing,” says Hunt, “models the spread of a novel allele. But the key is gene expression, not genotype.”

Thanks to a growing battery of analytical techniques, gene expression is something we can observe. The key to understanding those observations is what Sean Carroll of the University of Wisconsin has called the expanded evolutionary synthesis. But if its supporters are right, it may go down in the history of biology as the Third Synthesis, following the Modern Synthesis of the 1930s and the “selfish”-gene-centered synthesis of sociobiology in the 1960s and 1970s. At the heart of this latest synthesis is evolutionarydevelopmental biology, or evo-devo, a movement that emerged in the late 1990s and continues to grow today.

Amy Toth, a post-doc in genomic biology at the University of Illinois at Urbana-Champaign, says that many of the morphological differences among eusocial insects don’t arise from genes coding for body plan, but from differential nutrition. “For a long time,” she says, “people have known that nutritional differences are important in social insect societies. Queens are better nourished than other workers, and that’s very well established for many different species.” What Toth’s and others’ research is showing now is that there are nutritional differences among workers as well: “Skinny ones are foragers, and fat ones tend to do tasks in the nest, such as brood care,” she says. What’s more, they are able to trace the mechanisms behind those differences down to interactions on the genetic level.

Her work, along with that of Gene Robinson, also at the University of Illinois at Urbana- Champaign, and Jim Hunt, shows that it’s not merely differential nutrition that leads to caste differences, but the fact that differential nutrition affects gene expression. A poorly fed larva’s gene that codes for, say, vision will be expressed at a different intensity and at different times from one who is well fed. So the individual with more acute vision will, as an adult, undertake tasks for which vision is important. The two insects share a genotype, but because their genes are switched on or off at different times, their life cycles and even appearance would seem to be those of unrelated individuals. In ants, which are more sophisticated, differential gene expression leads to radical morphological differences, such as wide divergence in head and mandible size, and even the presence or absence of wings, all macroscopic differences that one would usually ascribe to genotype.

Hunt’s study of the eusocial paper wasps and their fairly simple colonies, enhanced by Robinson and Toth’s pioneering work in sequencing a partial paper wasp genome to compare with the completed honeybee genome, is useful for revealing one way in which eusociality, and sterility in particular, might have evolved.

The life cycle of a paper wasp colony begins with a foundress, a female wasp who, at the end of the previous autumn, mated with a single male and managed to survive the winter in hibernation. In spring, with the male’s sperm still living inside her, she begins to construct her nest, into which she deposits fertilized eggs that will become the first generation of female workers. As the larvae develop, the foundress feeds and cares for them, though not very well.

Hunt says the ones that are fed only by the foundress are poorly fed, and though they are destined not to reproduce, they are, surprisingly, not born sterile. “When they emerge,” he says, “they are reproductively ready to go. They have the physiology of a noneusocial, solitary wasp. They have their reproductive physiology switched on.”

But because they were poorly fed, they are not fully developed. Their bodies are soft, and they cannot fly for the first day or so, so they stay in the nest. This is something, Hunt says, that a solitary, noneusocial wasp would never do, and it has nothing to do with a mutation. Because their reproductive system is ginned up, this first generation is primed for maternal behavior; what they find while hanging around the nest is that there is a second generation of larvae already present and in need of nourishment. So because they cannot fly away and seek the food they need to develop their ovaries, they instead rear their mother’s young, their brothers and sisters. The energetic cost of mothering eventually causes their reproductive systems to shut down entirely, and they will remain sterile the rest of their lives.

On the other hand, the females of this second generation, which are called gynes, emerge from the larval state fat and healthy, but with their reproductive systems not yet active. They stay in the nest and continue to accept the attention and food provided by the workers. Toward the end of the summer, when the food sources start to dry up and the workers return to the colony with less and less to share with their siblings, the gynes will leave the nest and, if they are lucky, be inseminated. They will then hibernate, and, if they survive the winter, attempt to found their own colonies. Meanwhile, the worker will have died at home. Their life cycles could not be more different, though their genotypes are the same.

In Hunt’s view, kin selection — selection in related groups — and multilevel selection — selection among unrelated groups — each have a role to play in explaining the origin of eusociality. To illustrate how they might converge to evolve eusociality in a noneusocial species, says Hunt, consider the wood roach and its closest relative, the termite. Termites are fully eusocial, but the wood roach is not. It’s important to note that they are diploid, so whatever role the extra-close relatedness, resulting from haplodiploidy, might have in encouraging eusociality in Hymenoptera doesn’t apply here.

“A pair of wood roaches will excavate a chamber in a rotting log,” says Hunt, “and will rear a first brood. They do so in part by feeding the offspring with liquid from their anus, or cloaca, which is energetically so costly that they are rarely able to produce a second brood. That’s pretty much it.”

But, he says, if the brood were poorly fed, the parents might have enough energy left over from their shoddy parenting to produce a second brood. And if the first brood emerges with its reproductive systems ginned up from malnutrition, their maternal instincts will compel them to care for the second brood. The energetic costs of maternal care would cause their reproductive systems to stop developing, and they’d become workers. Our hypothetical wood roaches did not need to undergo millennia of fine-grained mutations to reach the threshold of eusociality.

But this uncontroversial hypothetical reveals the chasm that separates one theoretical interpretation from another. The way E.O. Wilson sees it, evolution would disregard the fact that those wood roaches are related at all. “All you need is a single preadaptation,” he says, that leads to progressive provisioning of young — shoddy parenting. “When that happens, you’ve reached the point where one small step can produce a eusocial colony. This isn’t dreaming. This is what scientists who work on this stage have learned.” A recent paper by Wilson cites, among others, biologists Shôichi F. Sakagami and Yasuo Maeta on this point. They found that they were able to induce division of labor in otherwise solitary bees by putting them in the same nest. “All you need is a single change,” Wilson argues. “One allele could do it, could cause the young and mother to stay at the nest and not disperse. Automatically, you start dividing labor.”

“Whoah,” says Crespi. “They stay at home with their mother, so you have a family. They don’t move in with a nonrelative to make a new home. Eusociality doesn’t evolve in groups of nonrelatives who might come together for whatever reason.”

Wilson’s Superorganism coauthor, Bert Hölldobler, sees it Crespi’s way.

“Here I totally disagree with Ed Wilson,” says Hölldobler. “He knows that. In order for eusociality to evolve, the beginning of eusociality, you need close relatedness or it wouldn’t work. And why Ed thinks this is not important remains a puzzle to me. We agree on 98 percent of everything. But you need close relatedness. Otherwise it’s hard to understand.”

Hunt occupies something of a middle ground, arguing that while relatedness is not important to bring a species to the threshold of eusociality, it is essential to carrying it over. Says Hunt, “Once you hit the threshold, evolution can incorporate multilevel selection on the group of relatives and you’re off to the races.” A lineage of wood roaches becomes eusocial, and after 100 millions years, maybe you get a superorganism.

Techniques from evo-devo and the Third Synthesis that allow us to observe gene expression have eliminated some, though clearly not all, of the interpretive fog that makes the enterprise of crafting theory so difficult. Theorizing in the absence of empirical data can take one only so far, and of all the eusocial species — wasps, bees, thrips, shrimp, mole rats, and so on — we have a complete genome of only one, the honeybee. As more are sequenced, the picture will become clearer, and theoretical differences will narrow. We will be able to lay the genomes of eusocial species over top of one another, from the primitive to the advanced, and what we see will be a projection of the 100 million years it takes to get from wood roach to leaf-cutter ant. And with luck, it won’t take until Darwin’s 300th anniversary to get there.

Originally published April 14, 2009

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