

A few years ago, I decided to fry up a mess of smallmouth bass from my parents' pond. But when we – okay, my mom – started to clean the fish, they were full of parasites.

After identifying them (thank you, Maine Fish & Wildlife Service!) I hopped online to learn more about the parasites. What I found was amazing.

The parasites, known as yellow grubs, have a very circuitous life cycle. The eggs are passed into the water by fish-eating birds like heron, then picked up by fish. The more parasites that infest a fish, the more likely it is to swim near the surface – making it more likely to be eaten by a bird, inside of which the parasites lay their eggs. And so the cycle of parasite life continues.

What caught my attention was the relationship between parasite population density and the odds of a fish being eaten. Clearly, natural selection favored those parasites whose interactions caused the fish to adopt the riskiest behaviors – but I'd always thought of evolution as a process that operated on individual adaptations, rather than group behaviors.

Talking with scientists, I learned that group selection is central to the storied, sometimes controversial field of superorganism theory, in which a population of creatures can be seen not as a collection of disparate individuals but as a high-level organism unto itself.

A leader in superorganism studies is Arizona State University's Bert Hoelldobler. I posted on his latest theory of evolution and altruism last month, and yesterday managed to get him on the phone. (On a side note, I had to call him at the office of E.O. Wilson, with whom he's writing a book on superorganisms.) I asked him to explain the history of superorganism theory, and he graciously obliged:

The history is complicated. In the early beginning of last century, it was William Wheeler and Alfred Emerson, two eminent entomologists, who compared insect societies to an organism. They didn't use the term superorganism, but said that each unit is like a cell in a body, or an organ. The reproductive units are the queens. The picture was very popular. It was taken over by philosophers, and all sort of things seen as superorganisms – a town, a city. But it became so exaggerated that it became useless, more a philosophical issue than a biological issue.

The biological concept of the superorganism then experienced a demise with the better understanding of sociogenetics – understanding that insect societies are not so homogeneous on a genetic basis. [...] For that reason, Wheeler's superorganism concept was demolished, not taken seriously anymore. The focus was more on the individuals in the colony

\– what is their selective advantage to not having offspring and taking care of the sisters. The more we understood about genetics, the more the focus was on the gene.

Then, with the burst of inclusive fitness theory, better known as kinship selection theory, came a shift of thinking. The work focused on how individual genes spread in a population, especially those genes, for example, that code for altruistic behavior, which the social insects have to the extreme. Honeybees commit hara-kiri for sake of the colony – this was a puzzle to us.

(Darwin had even said, if I don't resolve this problem, how such altruistic genes can be selected by natural selection, then the theory fails. How can altruistic traits be selected and propagated if those who show it don't reproduce? He said, unless I solve this problem, I can throw away whole theory.

Then Darwin found the solution: it was at that time a superorganism solution, but not in the Wheeler sense. Darwin said, the target of selection doesn't have to be individuals, but the group of the whole family. And, basically, he was right.)

But as population genetics developed in the 60s, when Hamilton's big papers came out, everyone focused on individuals and on the gene.

Richard Dawkins wrote The Selfish Gene, which was brilliant but totally gene-level. Richard even said, it's the gene that's selected. Classical evolutionary biologists say that selection works on the phenotype, the whole organism, and genes are the unit of selection. We see the change of gene frequencies, but the process of selecting is the whole organism.

Arguing back and forth, the British school [won]: it all depends on the gene. This has changed. Now, slowly, there was again a focus on the phenotype, which is affected by selection. Everyone agrees on this issue. Through selection, gene frequency changed. If a gene codes for a particular behavior, which gives the individual a carrier of the gene an advantage to reproducing, then identical copies represented in offspring. Individuals who are better-adapted will have more offspring.

But it's the individual, the carrier of this gene, who carries many other genes, that is exposed to selection. When we breed, we select whole animals. Now, slowly, guys like me and Ed Wilson who work on insects, began to say that the colony is the target of selection. We came under fire for this, but slowly it's been understood, now everyone agrees, that there is a multi-level selction: that selection can work on the individual, on the kin group, maybe even the group that is not a kin group.

So this is the theory. I'm an experimental behavioral biologist, my career committed to understanding the workings of insect societies: the mechanisms that make such a huge group of individuals, sometimes 20 million, work. I work on communication mechanisms, what regulates division of labor among reproductive individuals – and you cannot help but come back and see these highly evolved societies, like leafcutter ants, as an organism.

To be continued....